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Respiratory Patterns in Roots in Relation to Their Functioning
In Plant Roots. The Hidden Half (Y. Waisel, A. Eshel, and K. Kafkaki, Eds.). Marcel
Dekker, Inc. New York (2000)
Hans Lambers1,2, Owen K. Atkin3, and Frank F. Millenaar2
1Plant Sciences, The University of Western Australia, Crawley WA 6009, Australia;
2Plant Ecophysiology, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The
Netherlands; 3Department of Biology, University of York, PO Box 373, York Y01
5YW,York, United Kingdom
1
Table of contents
I INTRODUCTION
II THE QUANTITATIVE SIGNIFICANCE OF ROOT RESPIRATION AS A
FRACTION OF THE C-BALANCE OF THE PLANT
II.A Root respiration as a fraction of the photosynthates translocated to the roots
II.B Root respiration as a fraction of the photosynthates produced daily
III VARIATION IN ROOT RESPIRATION AS DEPENDENT ON ONTOGENY
AND SPECIES
III.A Variation in the rate of respiration
III.B Variation in the respiratory quotient
III.C Variation in capacity and activity of the alternative path
IV THE REGULATION OF ROOT RESPIRATION
IV.A Short-term effects
IV.A.1 Partitioning of electrons between the cytochrome path and the alternative
path: overflow or competition
IV.A.2 Regulation of glycolysis and electron transport
IV.A.3 Partitioning of electrons between the two internal NADH dehydrogenases
IV.A.4 Regulation by carbohydrate supply
IV.B Long-term effects
IV.C Diurnal fluctuations in root respiration
IV.D Effects of plant hormones
IV.E Conclusions
V QUANTIFICATION OF THE REQUIREMENT FOR RESPIRATORY
ENERGY FOR ANION UPTAKE, GROWTH AND MAINTENANCE OF
ROOTS
V.A Methodology
V.B Variation between species and environmental conditions
VI THE ALTERNATIVE PATH: ITS CONTRIBUTION TO RESPIRATION AND
ITS POSSIBLE SIGNIFICANCE IN THE FUNCTIONING OF ROOTS
VI.A Assessment of alternative path activity
VI.B. The physiological significance of the alternative path
VII EFFECTS OF ENVIRONMENTAL CONDITIONS
VII.A Abiotic factors
VII.A.1 Nutrient supply
VII.A.2 pH
VII.A.3 Aluminum
VII.A.4 Heavy metals
VII.A.5 Salinity and drought
VII.A.6 Temperature
VII.A.7 Light conditions
VII.A.8 Partial pressures of O2 and CO2 in the rhizosphere
VII.B Biotic factors
VII.B.1 Effects of symbiotic organisms
VII.B.2 Effects of parasitic organisms
VIII CONCLUDING REMARKS
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I. INTRODUCTION
A significant portion of the carbohydrates that are produced daily in photosynthesis are
respired in the roots. The magnitude varies with age of the plants, growth conditions,
and the species under investigation. The rate of root respiration, measured as O2
consumption or CO2 release, also varies between species, even when plants are grown
under very similar conditions. This chapter discusses factors that are responsible for the
differences in root respiration.
An important feature of the respiration in higher plants is the participation of an
alternative, nonphosphorylating electron-transport path, which decreases the efficiency
of ATP production in respiration (Lambers, 1985). Since the nonphosphorylating path
can be a major sink for carbohydrates, the regulation of the activity of this path warrants
an extensive discussion.
Respiratory energy is the driving force for biosynthetic reactions, as well as for
maintenance and transport processes. In recent years more information has become
available on the quantitative significance of the various sinks for respiratory energy.
Methods that are employed in this area of research and data that have been obtained in
this manner will receive attention.
Finally, both genetic and environmentally induced variation in root respiration is
discussed in the light of the functioning of the whole plant.
II. THE QUANTITATIVE SIGNIFICANCE OF ROOT RESPIRATION AS A
FRACTION OF THE C-BALANCE OF THE PLANT
Between one quarter and two thirds of all the photosynthates produced per day are
respired in the same period (Poorter et al., 1990; Van der Werf et al., 1994). A major
portion of this respiration occurs in the roots, connected with their growth and
maintenance and with the absorption of ions (see section V.B).
A. Root respiration as a fraction of the photosynthates translocated to the roots
Between one and two thirds of all the carbohydrates that are translocated to the roots are
used in respiration (Table 1). This fraction tends to increase with increasing plant age, as
a consequence of a decreased translocation of assimilates to the roots and is partly due to
the proportionally greater amount of maintenance energy required when root growth
slows down (see section V).
The proportion of carbohydrates that are respired in the roots increases when growth
occurs at a low nutrient supply (Van der Werf et al., 1992a; Table 1). This is largely
explained by the slower growth of roots at a limiting supply of nutrients; in addition
3
specific costs for maintenance or ion uptake might increase (Van der Werf et al., 1994).
B. Root respiration as a fraction of the photosynthates produced daily
Eight to 52% of all carbohydrates produced per day in photosynthesis are respired in the
roots during the same period (Table 2). This percentage increases with decreasing
growth rate of the plants, be it due to an inherently low growth potential of the species
(Poorter et al., 1990; Atkin et al., 1996) or to growth being restricted by a suboptimal
nutrient supply (Boot et al., 1992; Van der Werf et al., 1992a). The percentage tends to
decrease with increase in age. This decrease is probably not associated with an increased
efficiency of respiration, since the contribution of the nonphosphorylating, alternative
path in root respiration of Glycine max (L.) Merr increases with increasing age of the
plants (Millar et al., 1998). Therefore, this decrease may be due to a decrease in the
demand for respiratory energy (e.g., in Carex acutiformis Ehrh., where the energy
required for root growth and ion uptake decreases drastically with increasing age; Van
der Werf et al., 1988).
The fraction of carbohydrates that is used in root respiration, including the respiration of
microsymbionts, if present, is affected by both abiotic and biotic environmental factors
(Table 2). In the presence of an N2-fixing symbiont (Rhizobium), carbohydrate
utilization by root respiration is greater than that of nonnodulated roots, supplied with
nitrate as the source of nitrogen. This is explained by the greater energy requirement for
N-assimilation during N2-fixation in comparison with that for NO3--assimilation (see
section VII.B). Also in the presence of a symbiotic mycorrhizal fungus (Glomus
mosseae (Nicol. and Gerd.) Gerd. and Trappe) the fraction of carbohydrates used in root
respiration of Allium porrum L. is larger than that of nonsymbiotic plants (Table 2).
It is well documented that during growth at a low light intensity, the rate of root
respiration is relatively low (Lambers and Posthumus, 1980; Kuiper and Smid, 1985).
Less information is available on the effects of light intensity during growth on the
contribution of root respiration to the plant’s total carbon budget. Long-term exposure to
a combination of reduced light intensity and short days has very little effect on the
fraction of carbohydrates that are used in root respiration of Cucumis sativus L. (Table
2; Challa, 1976). Poorter (1991) found that approximately 30% of all the photosynthates
produced per day are respired in the roots of Deschampsia flexuosa (L.) Trin. and
Holcus lanata L., whether the grasses were grown at high or at low irradiance.
The wide variation in the fraction of carbohydrates that are translocated to the roots and
subsequently respired (Table 1) is partly associated with variation in the growth rate of
the roots (Fig. 1). Slow-growing plants consume a far greater proportion of the daily
produced photosynthates in root respiration than fast-growing ones. This is true for a
comparison of species which vary in their potential growth rate (Poorter et al., 1990;
Atkin et al., 1996), as well as for a comparison of plants of the same species which vary
in growth rate, due to variation in the nutrient supply (Van der Werf et al., 1992a).
Compared with fast-growing species, roots of inherently slow-growing species have
relatively large costs for nitrate uptake, due to a major nitrate efflux component
4
(Scheurwater et al. 1998, 1999). A similar explanation may apply for plants that grow
slowly due to a limiting nitrate supply, but further experiments are required to confirm
this (Lambers et al. 1998a).
III. VARIATION IN ROOT RESPIRATION AS DEPENDENT ON ONTOGENY
AND SPECIES
It is well documented that both the rate of root respiration and the respiratory quotient
may vary between species, environmental conditions and ontogeny. In this section we
will analyze this variation and its consequences for the roots’ costs of functioning.
A. Variation in the rate of respiration
It has been known for a long time that the rate of respiration of the primary root varies
with distance from the tip. Machlis (1944) found a gradual decline of both the rate of
oxygen uptake and that of carbon dioxide release (expressed on a root volume basis) for
the primary root of Hordeum vulgare L. seedlings. The rates are 2 to 3 times higher in
the root tip than at a distance 90 mm from the tip. Similarly, the rate of oxygen uptake
(expressed on a fresh mass basis) of the 10 to 15 mm segment of Allium cepa L. roots is
40% less than that of the apical 0 to 5 mm (Berry and Brock, 1946).
A partial explanation for the decreasing respiration rate (on a volume or fresh mass
basis) with increasing distance from the tip is offered when the data are expressed on a
dry mass basis and per cell (Goddard and Bonner, 1960). This shows that the higher
respiration rate, per unit fresh mass, in the tip, is due to the lower water content of the
smaller, meristematic cells in this region. Expressing the data on a dry mass basis leaves
very little variation in the respiration rate. In Allium cepa roots, the respiration per cell
and per gram nitrogen is very low in the smaller cells closest to the tip (Wanner, 1950;
Fig. 2). It is about three times higher in the 2 to 5 mm zone than closer to or further
away from the tip. In Allium cepa, this is the zone where cell elongation and synthesis of
protein and nucleic acids (both DNA and RNA) are most pronounced (Yemm, 1965).
Presumably the high respiration rate in this zone is due to the high requirement for
respiratory energy for biosynthetic and uptake processes, as this is a major factor
regulating the rate of respiration (see section IV.A.2). Thus, variation in respiration
along the primary root axis has a distinct physiological basis and is clearly understood
when the data are expressed on the proper basis. However, it should be borne in mind
that the data discussed here pertain to the primary (growing) root. No data are available
on respiratory patterns in lateral roots, which may be of particular interest because of
their restricted growth period. Consequently, there is still very little information on the
partitioning of respiratory activity over the entire root system.
Rates of root respiration vary widely among species (Table 3). Although fast-growing
plants use less carbon in root respiration (expressed as a fraction of the carbohydrates
fixed in photosynthesis on a daily basis) than slow-growing ones, their rates of root
5
respiration are higher, especially when expressed on a dry mass basis (Poorter et al.,
1991; Van der Werf et al., 1992a; Atkin et al., 1996).
The variation in the rate of root respiration (Table 3 and Fig. 2) is largely due to
differences in the demand for respiratory energy, e.g., for ion uptake and growth, rather
than differences in respiratory efficiency. However, the specific energy requirements for
ion uptake, growth or maintenance may differ as well (see section V).
B. Variation in the respiratory quotient
The respiratory quotient (RQ) of root respiration varies with the potential growth rate of
a species and depends on the source of N (NH4+, NO3- or N2; Table 4). In the absence of
biosynthetic processes, the RQ of root respiration is expected to be 1.0, if sucrose is the
only substrate for respiration. For roots of young seedlings, measured in the absence of a
N source, values close to 1.0 have indeed been found (Table 4). The RQ may be greater
than 1, if more oxidized substrates, e.g., organic acids, are an additional substrate.
Organic acids (malate) may be produced concomitant with the reduction of nitrate in
leaves, followed by their transport and decarboxylation in the roots (Ben Zioni et al.,
1971). If nitrate reduction proceeds in the roots, the RQ is also expected to be greater
than 1, since per molecule of nitrate reduced to ammonium an additional 2 molecules of
CO2 are produced. During synthesis of biomass, both carboxylating and decarboxylating
reactions occur, which also affect the RQ. For example, synthesis of oxidized
compounds such as organic acids decreases the RQ, whereas the production of reduced
compounds such as lipids leads to higher RQ values. Comparing the molecular formula
of the biochemical compounds of the biomass with that of sucrose, RQ values greater
than 1 are expected. The RQ will be less than 1, if compounds that are more reduced
than glucose, e.g., lipids and protein, are an additional substrate. This may happen upon
starvation of excised root tips (Table 4; Saglio and Pradet, 1980; Brouquisse et al.,
1991).
Like other slow-growing species from nutrient-poor habitats, the slow-growing Festuca
ovina L. has a low RQ compared with those of the faster-growing Dactylis glomerata L.
and Holcus lanatus (Table 4; Scheurwater et al., 1998). Taking into account the
respiratory energy costs of biomass synthesis from glucose, ammonia and minerals,
Penning de Vries et al. (1974) calculated a value for RQ of 1.25. Since respiration
associated with transport processes and maintenance proceeds with a RQ of 1.0, lower
values are expected for total root respiration if NH4+ is the source of N. Fast-growing
plants require a greater proportion of root respiration for growth (up to 45%), whereas
slow-growing ones use proportionally more for transport and maintenance (up to 82%;
Poorter et al., 1991). However, this would lead to RQ values, with ammonium being the
N source, as different as 1.11 and 1.05 for fast- and slow-growing species, respectively.
Faster-growing species also have higher specific rates of nitrate reduction in their roots
than slow-growing species, which offers an additional explanation (Scheurwater 1999).
If the fast-growing species were to make greater use of the malate shuttle, i.e.
decarboxylate relatively more malate and exchanging the resultant HCO3- for nitrate and
take up relatively less K+ (Ben Zioni et al., 1971), then this might also partly account for
6
their higher RQ values. However, on the basis of an analysis of their cation, anion and
organic N contents, H. Poorter (pers. comm.) concluded that fast- and slow-growing
species do not differ in the proportion of NO3- that is reduced in the root. Using several
approaches to assess nitrate reductase activity in roots and shoots, Scheurwater (1999)
confirmed such a similar pattern in inherently fast- and slow-growing grass species. An
additional factor that accounts for lower RQ values in slow-growing species is their
relatively inefficient nitrate-uptake system, when plants are grown with free access to
nitrate (see section VB). Since this additional respiration proceeds with an RQ of 1.0, it
has the net effect of lowering the overall RQ value. We conclude that the relatively high
RQ of fast-growing species reflects a rapid rate of nitrate reduction in these roots
compared with those of slow-growing species as well as a more efficient nitrate-uptake
system.
C. Variation in capacity and activity of the alternative path
A substantial number of studies have investigated the level of alternative pathway
respiration in roots, using respiratory inhibitors such as salicylhydroxamic acid (SHAM;
a specific inhibitor of the alternative oxidase) and KCN (a specific inhibitor of the
cytochrome pathway). These studies showed that there is a wide variation in the KCN-
resistant component of respiration that is sensitive to SHAM (Table 3). The use of these
inhibitors was based on the assumption that the cytochrome pathway is always fully
saturated whenever the alternative pathway contributes to respiration (see section VI.A).
However, recent studies have demonstrated that the alternative pathway actually shares
electrons that are donated by reduced ubiquinone with the cytochrome pathway. As a
result, the cytochrome pathway does not have to be fully saturated for the alternative
pathway to become engaged (Hoefnagel et al., 1995; Ribas-Carbo et al., 1995; Wagner
and Krab, 1995; Day et al., 1996). Previous estimates of alternative pathway respiration
using the inhibitor SHAM may, therefore, have resulted in substantial underestimates of
alternative pathway activity.
To accurately estimate alternative pathway respiration in intact roots, the oxygen–
isotope fractionation technique (Guy et al., 1989, 1992; Henry et al. 1999) needs to be
used. However, only a few studies have used this technique to estimate alternative
pathway activity in roots (Millar et al. 1998; Millenaar et al. 2000a,b). Millar et al.
(1998) showed a gradual decline in activity of the alternative path with increasing age of
the roots of Glycine max, while Millenaar et al. (2000b) found that alternative pathway
respiration represents a greater proportion of total root respiration in inherently fast-
growing species compared with their slow-growing counterparts. The activity of the
alternative pathway remains constant in roots exposed to long nights and short days,
following transfer from high light/short nights (Millenaar et al. 2000a).
Variation in the activity of the nonphosphorylating alternative path alters the roots’ costs
of functioning to a significant extent. When only the cytochrome path contributes to root
respiration, the ATP yield per O2 taken up is three times greater than when respiration is
entirely due to the activity of the alternative path (Table 5). In vivo, the ADP:O ratio is
likely to vary between 3 and 1 (Lambers, 1995). It is therefore important that further
7
work using the 18O isotope-fractionation technique be conducted to determine the extent
to which alternative pathway activity varies in roots.
IV. THE REGULATION OF ROOT RESPIRATION
A. Short-term effects
The rate of root respiration responds both to the demand for respiratory energy and the
carbohydrate supply (Lambers et al., 1998b). These are rapid effects that can be
explained by the response of specific enzymes and/or the electron-transport systems. To
understand the rapid responses upon changes in the environment, the regulation of root
respiration is discussed in some detail below.
1. Regulation by carbohydrate supply
Challa (1976) found a diurnal fluctuation both in the level of soluble sugars (Fig. 3a)
and in CO2-production (Fig. 3b) for roots of Cucumis sativus, grown under conditions of
a low light intensity and a short day. No such fluctuation in root respiration of C. sativus
(Challa, 1976) and of four grass species (Scheurwater et al. 1998) is found when the
plants are grown at a high light intensity and a long day. Plants grown under such
conditions have a high level of carbohydrates in their roots throughout the entire day.
Respiration of Zea mays root tips, depleted of sugars, is stimulated by 0.2 mol m-3
exogenous glucose (Saglio and Pradet, 1980; Brouquisse et al., 1991). Bryce and ap
Rees (1985a) also found such a stimulation of respiration for the apical 40 mm roots of
Pisum sativum by exogenous sucrose (25 to 100 mol m-3; Fig. 4), even without depleting
them of substrate. The effect of exogenous sucrose on pea root respiration increases with
increasing time of exposure. This points to adjustment of the respiratory apparatus,
similarly to what has been found for roots of intact plants (see section IV.B). Exogenous
sugars do not invariably stimulate the rate of root respiration (Farrar, 1981). This is
unlikely to be due to poor absorption of the added sugars. Rather, it reflects the
adjustment of the respiratory capacity to the root’s carbohydrate level (see section IV.B).
Root respiration is regulated by adenylates and/or by the level of respiratory substrate.
Adenylate control of electron transport and/or of glycolysis often coincides with
regulation by the availability of substrate.
2. Regulation of glycolysis and electron transport
Glycolysis in roots is controlled by ‘energy demand’ (Lambers, 1985). This is largely
due to the allosteric regulation of two key enzymes, phosphofructokinase and pyruvate
kinase, by adenylates. This regulation explains the ‘Pasteur effect’, i.e. the stimulation of
glycolysis under low-oxygen conditions, when oxidative phosphorylation is curtailed
and the level of ATP drops, whereas that of ADP increases. Adenylates do not only
exert control over glycolysis, but also over mitochondrial electron transport.
8
Saturation of the cytochrome path may be due to a limiting capacity of the electron-
transport chain per se. Alternatively, it may be due to a restriction of the flux of
electrons through the cytochrome path by oxidative phosphorylation. In the absence of
ADP, the proton-motive force across the inner mitochondrial membrane increases, and
so restricts the flow of electrons to O2. This can be analyzed in vivo by application of an
uncoupler (e.g., DNP, CCCP, FCCP, or preferably S13; Lambers, 1995) in the presence
of an inhibitor which fully blocks the alternative path (e.g., SHAM). If addition of an
uncoupler stimulates respiration in the presence of SHAM, then the cytochrome path
was restricted by adenylates when the alternative path was blocked. However, these
results cannot show if the cytochrome path was similarly controlled when the alternative
path is not inhibited, because inhibition of the alternative path may have shifted electron
flow toward the cytochrome path. If SHAM does not inhibit respiration, and an
uncoupler does not stimulate oxygen uptake, mitochondrial electron flow is not
restricted by adenylates, but limited by the supply of respiratory substrate. In intact roots,
mitochondria often operate in a state where ADP is present in a concentration which
restricts the flow of electrons through the cytochrome path to a greater or lesser extent
(Millar et al. 1998; see section IV.A.1).
If the addition of an uncoupler, e.g., DNP or FCCP, stimulates the rate of respiration in
the absence of an inhibitor of the alternative path, respiration must have been limited by
adenylates. However, this does not imply a limitation of oxidative phosphorylation by
ADP. Rather, it may be the substrate supply to the mitochondria which is restricted by
adenylates, e.g., via the control of glycolysis. Table 6 shows that adenylates control the
rate of oxygen uptake in Zea mays L. roots via an effect through limitation of the flux of
electrons through the respiratory chain. In contrast, adenylates control respiration in
roots of Phaseolus vulgaris L. via the substrate supply to the mitochondria, presumably
via their effect on glycolysis (‘Pasteur effect’; Day and Lambers, 1983).
The relief of ADP limitation of the cytochrome path does not only enhance the flux of
electrons through this path, but may also decrease the electron flow through the
alternative path. Respiration is not invariably controlled by adenylates. Respiration of
Zea mays root tips, depleted of sugars, cannot be stimulated by uncoupler (Saglio and
Pradet, 1980; Williams and Farrar, 1992). Uncoupler only has an effect in the presence
of a high endogenous level of sugars and when glucose is exogenously supplied. Thus
adenylate control is more important at a high level of endogenous respiratory substrate
than at low levels.
3. Partitioning of electrons between the two internal NADH dehydrogenases
Internal NADH, i.e. NADH originating in the tricarboxylic acid cycle, can be accepted
by the electron-transport pathway via two internal NADH dehydrogenases, both located
in the inner mitochondrial membrane. Electron transport from internal NADH to
ubiquinone via the rotenone-sensitive dehydrogenase is coupled to proton extrusion, and
hence to oxidative phosphorylation. Electron transport via the rotenone-resistant internal
dehydrogenase is not coupled to proton extrusion.
9
The Km of the internal rotenone-sensitive dehydrogenase is an order of magnitude lower
than that of the resistant one (Møller and Palmer, 1982; Agius et al., 1998). This lower
affinity together with the lack of any association with proton extrusion of the rotenone-
resistant dehydrogenase suggest that it is operative when the NADH/NAD ratio is high,
or when the availability of ADP is low. Thus it appears that the rotenone-insensitive
path can only become engaged in the presence of a high level of NADH in the
mitochondria. However, so far there is no information on the operation of the rotenone-
insensitive path in intact roots. In the absence of any suitable inhibitor of the rotenone-
insensitive bypass such evidence will be hard to obtain.
4. Partitioning of electrons between the cytochrome path and the alternative path:
overflow or competition
The existence of two mitochondrial respiratory pathways, both transporting electrons
from NADH, produced inside the mitochondria, to oxygen, raises the question how the
diversion of electrons between these paths is regulated. This is particularly relevant,
since transport of electrons via the cytochrome path is coupled to proton extrusion and
hence oxidative phosphorylation. In contrast, transport of electrons to O2 via the
alternative path is not coupled to the generation of a proton-motive force, at least not
beyond the branching point with the cytochrome path, i.e. ubiquinone.
Bahr and Bonner (1973a; 1973b) initially concluded that simple competition for
electrons between the alternative pathway and the cytochrome pathway cannot explain
the experimental data obtained with isolated mitochondria. This manner of partitioning
of electrons between the two electron-transport pathways could be explained by the
differential response of the cytochrome path and the alternative path to their common
substrate, i.e. reduced ubiquinone. In mitochondria isolated from cotyledons of Glycine
max (L.) Merr, the activity of the cytochrome path increases linearly with the fraction of
ubiquinone that is in its reduced state. In contrast, the alternative path shows no
appreciable activity until a substantial (30-40%) fraction of the ubiquinone is in its
reduced state, after which the activity increases very rapidly (Dry et al., 1989).
Until recently, the widely held view was that the alternative path invariably acts as an
‘overflow’ and never shares electrons with the cytochrome path. However, it has now
been established that the activity of the cytochrome path can increase upon inhibition of
the alternative path and that the electron-transport pathways share electrons from
reduced ubiquinone (see section VI.A).
B. Long-term effects
The respiratory apparatus can be modified by the internal and/or by the external
environment of the plant. These are relatively slow responses (several hours), compared
with the fast responses discussed in section IV.A. They are likely to significant in the
plant’s response to environmental factors such as light and nutrients.
After the removal of all but one seminal root of Hordeum distichum seedlings, the
soluble sugar concentration and respiration of the remaining seminal root increase
10
(Farrar and Jones, 1986). After pruning of the shoot to one leaf blade, both the soluble
sugar concentration and the respiration of the seminal roots decrease. The effects on
respiration reflect the coarse control of the respiratory capacity upon pruning or sucrose
feeding (Bingham and Farrar, 1988; Williams and Farrar, 1990).
Changes induced by pruning are due to long-term responses of the roots’ respiratory
metabolism to the carbohydrate supply (Fig. 4). The protein pattern of the roots of
pruned plants is affected within 24 h (Williams et al., 1992). Mitochondria isolated from
such roots show changes in respiratory properties and activities of cytochrome oxidase
(McDonnel and Farrar, 1992). Glucose feeding to leaves enhances the activity of several
glycolytic enzymes in these leaves, due to regulation of gene expression by carbohydrate
levels (Krapp and Stitt, 1994).
C. Diurnal fluctuations in root respiration
When plants are grown at a constant temperature, a relatively high light intensity and a
long photoperiod, the rate of root respiration tends to be rather constant throughout the
day (Challa, 1976; Veen, 1977; Fig. 3). However, this is not invariably so, and diurnal
patterns in CO2 production by roots have been recorded (Neales and Davies, 1966;
Osman, 1971). At a high photon input, diurnal patterns in CO2 production are unlikely
to be due to fluctuations in the level of carbohydrates (Huck et al., 1962; Farrar, 1981).
Rather, they tend to correlate with the rate of ion uptake (Huck et al., 1962; Hansen,
1980; Casadesus et al., 1995).
Root respiration is not a simple function of the carbohydrate supply from the shoot.
When both CO2 production and O2 consumption are measured, the latter tends to show
less diurnal variation (Fig. 5). Possibly, the variation in CO2 production is associated
with that in nitrate reduction in the roots. Additionally, it may be associated with
variation in the excretion of bicarbonate, which is released upon decarboxylation of
malate that is produced in the leaves, coupled to nitrate reduction, and subsequently
transported via the phloem to the roots (Ben Zioni et al., 1971).
Like root growth, the rate of ion uptake, though correlated with the carbohydrate supply
from the shoots, does not simply depend on carbohydrates because these are the source
of energy for uptake (Bowling, 1981). Bowling (1981) concluded that ion uptake in
Helianthus annuus L. is controlled by an ‘ion uptake controller’, imported from the
shoots. Both amino acids (Imsande and Touraine, 1994) and glutathione (Lappartient et
al., 1999), which are imported via the phloem, are such controlling factors.
Simultaneous changes in the rates of ion uptake and root respiration, therefore, probably
reflect the regulation of respiration by adenylates (‘energy demand’). Most likely, also
root growth, though correlated with the supply of carbohydrates from the shoot, is
regulated, rather than actually limited by this supply (McDonnel and Farrar, 1992).
We conclude that the diurnal variation in root respiration in plants grown under
constant-temperature conditions is a reflection of variation in the energy demand for
growth and ion uptake. However, if respiration is controlled by the demand for
11
respiratory energy, the question remains how the variation in this demand originates.
This question cannot yet be answered but is of obvious interest to those attempting to
model the growth of roots as dependent on carbohydrate supply and ion uptake.
D. Effects of plant hormones
Little work has been done on the effects of plant hormones on root respiration. Some
more data are available for other tissues and for isolated mitochondria. However, in the
latter case the concentrations required may indicate that the effects which have been
reported are not physiologically relevant. Only a brief survey on effects of plant growth
substances on respiration is provided here.
Markhart (1982) found an increase in CO2 production by Glycine max roots upon
exposure to ABA. During 6 hours of exposure to 44 mmol m-3 cis-trans or 60 mmol m-3
trans-trans ABA, root respiration gradually rises to 130% of the original value. In the
absence of more information on which respiratory pathway is stimulated by ABA and on
other aspects of carbohydrate transport and metabolism, a satisfactory explanation for
this effect of ABA on root respiration cannot yet be given.
Respiration of slices of storage tissue of Beta vulgaris L. roots (Palmer, 1966) increases
upon aging. This increase is prevented in the presence of 50 to 1000 mmol m-3 kinetin.
Since the rate of respiration decreases parallel to that of phosphate absorption, the effect
of kinetin on respiration may result from a decreased demand for metabolic energy for
phosphate uptake. Benzyladenine (10-8 mol m-3), a synthetic cytokinin applied to the
roots of Plantago major L., delays the decrease in root respiration found upon transfer
from a solution with an optimum nutrient supply to a solution where nutrients are
limiting (Kuiper and Staal, 1987). In these roots, cytokinins probably increase the roots’
demand for metabolic energy for ion uptake and thus account for the higher rate of
respiration in roots exposed to benzyladenine.
A number of cytokinins inhibit the oxidation of NADH by submitochondrial particles,
but not by intact mitochondria (Miller, 1980; 1982), suggesting that only the oxidation
of NADH originating in the tricarboxylic acid cycle, and not that of external NADH, is
inhibited. The cytokinins are effective in the range of 50 to 500 mmol m-3, which is
rather high compared with other known physiological effects of these hormones, e.g., on
root growth and aerenchyma formation of Zea mays roots, where kinetin is already
effective at 10 mmol m-3 (Konings and De Wolf, 1984). Preincubation of isolated
mitochondria in cytokinin solutions for several minutes does not lower the effective
concentration, so that it remains obscure if these effects have any physiological
relevance. Benzylaminopurine and several adenine analogues, with or without cytokinin
activity, inhibit the alternative path (Dizengremel, 1982; Miller, 1982). Titrations with
benzyladenine mimic those obtained using SHAM, but the effective concentration is
high: between 100 and 1000 mmol m-3.
Exposure of Solanum tuberosum tubers to ethylene (10 ppm) causes an upsurge of their
respiration rate (Reid and Pratt, 1972). The rate rapidly rises to 5 to 10 times the level of
12
control tubers within 30 h and then slowly falls. Treatment of potato tubers (Solomos
and Laties, 1976; Rychter et al., 1978) with ethylene enhances the capacity of the
cyanide-resistant path in mitochondria isolated from these tissues. The extent of the
increase depends on duration of the exposure and on the concentration of ethylene. The
physiological meaning of such high concentrations of ethylene on the alternative path
remains obscure; it is presumably linked to an increased demand for metabolic energy,
e.g., associated with the synthesis of specific proteins (Christofferson and Laties, 1982).
Respiration of the storage tissue of beet (Beta vulgaris L.) roots decreases in the
presence of 1 mol m-3 indolylacetic acid or other auxins. The rate of phosphate
absorption also decreases in the presence of these compounds, be it not in parallel
(Palmer, 1966). A partial explanation for the decreased respiration may be the decreased
demand for metabolic energy. However, since phosphate absorption and root respiration
did not decrease in the same manner for all auxins, this is unlikely to be the full
explanation. Neither respiration nor phosphate absorption by the storage tissue of Beta
vulgaris roots are significantly affected by gibberellin (Palmer, 1966).
The above compilation of effects of plant growth substances on respiration does not lead
to a complete model on cause and effects. Some of the effects described above may lack
physiological relevance. Others can possibly be explained by a modified requirement for
metabolic energy or by changes in allocation of carbohydrates to the roots. The effects of
environmental conditions on root respiration (see section VII) might be mediated by
hormones, but no clear-cut correlations are available.
E. Conclusions
The current view is that root respiration is controlled by a delicate balance between the
roots’ demand for ATP (adenylate control) and the availability of respiratory substrate.
Adenylates exert their effect both on glycolysis and on the activity of the cytochrome
path. Whenever the availability of substrate is large compared with the demand for ATP,
e.g., at low temperatures or upon a sudden increase in carbon flow to the roots, firstly,
the alternative path may become increasingly engaged. In the long term, the higher
availability of respiratory substrate enhances the capacity of various components of the
respiratory apparatus, due to gene transcription followed by de novo protein synthesis.
It should be kept in mind that many of the elements leading to the present model on the
regulation of root respiration need further investigation. For example, the change in
oxidation-reduction of the disulfide bonds of the alternative oxidase in intact roots so far
has only been studied in roots of Glycine max (Millar et al., 1998) and a range of Poa
species (Millenaar et al., 2000b). The in vivo activity of the alternative oxidase can
change without a change in the disulfide bonds of the alternative oxidase or in the
regulation by pyruvate or other organic acids (Millenaar et al., 1998, 2000b). Therefore,
although our understanding of the regulation of root respiration has increased
dramatically in the last decade, far more work needs to be done before a solid model can
be constructed.
13
V. QUANTIFICATION OF THE REQUIREMENT FOR RESPIRATORY
ENERGY FOR ANION UPTAKE, GROWTH AND MAINTENANCE OF
ROOTS
The first methods to quantify the various energy-requiring processes in roots, discerned
only two components of root respiration, i.e. respiration for growth, which included that
for ion uptake, and respiration for the maintenance of root biomass. Subsequent methods
included ion uptake as a third major process requiring respiratory energy (Veen, 1980).
Most investigators have not accounted for the engagement of the alternative path. Since
variation in the requirement of respiratory energy might be due to variation in the
engagement of the alternative path, and since the contribution of this pathway to total
root respiration may vary with age (Millar et al., 1998), the energy requirement of roots
has been expressed in terms of ATP, rather than O2 (Lambers and Van der Werf, 1988).
However, most of these data have been obtained using inhibitors to assess alternative
path activity, which makes the conversion from oxygen to ATP invalid.
A. Methodology
The rate of root respiration depends on three major energy-requiring processes, i.e.
maintenance of root biomass, root growth and ion uptake. This can be summarized in
the following overall equation (Lambers et al., 1998b):
r = rm + 1/Ygrowth RGR + 1/Utransport TR
where r is the rate of root respiration (µmol O2 or CO2 g-1 day-1); rm is the rate of root
respiration to produce ATP for the maintenance of biomass; 1/Ygrowth (mmol O2 or CO2
g-1) is the root respiration to produce ATP for the synthesis of cell material; RGR is the
relative growth rate of the roots (mg g-1 day-1); 1/Utransport (mol O2 or CO2 mol-1) is the
rate of respiration required to support TR, the transport rate (µmol g-1 day-1). In roots
TR, equals the net ion uptake rate (NIR) and the rate of xylem loading.
The respiratory energy requirement for maintenance of root biomass is assumed to be
linearly related to the fresh or dry mass of the root biomass to be maintained. Similarly,
it is assumed that the respiratory energy requirement for anion uptake is proportional to
the amount of anions taken up, whereas that for root growth is assumed to be
proportional to the relative growth rate of the roots. Thus, the specific costs for all three
processes are assumed to be constant during the experimental period.
Based on these assumptions, the rate of respiration per gram of roots can be related to
the relative growth rate of the roots and the rate of anion uptake by the roots.
Superimposed is the maintenance respiration. If there is no tight correlation between
growth and ion uptake, the costs of the three processes can be determined using a
multiple regression analysis (Van der Werf et al., 1988). The analysis is graphically
presented in a three-dimensional graph for the data of two Carex species (Fig. 6a). The
dotted plane gives the rate of root respiration (y-axis) as a function of both the relative
14
growth rate of the roots (z-axis) and the net rate of anion uptake by the roots (x-axis).
Since the specific costs for maintenance are assumed to be constant, it appears as the
intercept of the plane with the y-axis. The plane intersects both the y-z plane and the x-z
plane. The slope of the plane with the x-axis and the z-axis give 1/Ygrowth, and 1/Utransport,
respectively.
Since the processes of root growth and ion uptake are often tightly correlated, it may be
necessary to perturb the growth of a plant by pruning roots or shoots to discriminate
between the three processes (Bouma, 1995). Alternatively, a linear regression can be
carried out and the rate of root respiration can be plotted against the roots’ relative
growth rate. In such a plot, the intercept with the y-axis gives the rate of maintenance
respiration, whereas the slope includes costs for both root growth and for ion uptake.
Fig. 6b shows an example for roots of Quercus suber L. (Mata et al., 1996).
B. Variation between species and environmental conditions
Very few multiple regression analyses of the kind depicted in Fig. 6a have been carried
out, because of tight correlations between growth and ion uptake, forcing authors to take
refuge in an analysis as given in Fig. 6b. However, we can be quite sure that the specific
costs for one or more of the three major energy-requiring processes vary both between
species (Poorter et al., 1991) and between growth conditions (Van der Werf et al.,
1994). This conclusion is based on the observation that the rate of root respiration tends
to vary considerably less than that of growth and ion uptake, both among species with
different growth potential (Poorter et al., 1991, Atkin et al., 1996, Scheurwater et al.,
1998) and among plants with different N supply (Granato et al., 1989; Van der Werf et
al., 1992a).
The construction costs per unit biomass may vary with the chemical composition of the
plant. The oxygen requirement for the synthesis of roots of fast-growing species is
higher than that for slow-growing ones, due to their higher protein content (Poorter et
al., 1991) and hence does not account for the relatively high rates of respiration of
species with a low growth potential.
The specific costs for ion uptake are considerably greater for plants with a low growth
potential than for fast-growing ones (Scheurwater et al., 1998; Fig. 7), due to the
relatively greater importance of nitrate efflux (Scheurwater et al., 1999, Mata et al.,
2000). This explains the relatively high rate of respiration of inherently slow-growing
plants grown with free access to nutrients. There is also some indirect evidence that the
specific costs for ion uptake increase with a decline in growth rate due to greater
limitation by the nitrogen supply (Van der Werf et al., 1994, Lambers et al., 1998a).
Such variation in specific costs with variation in the rate of nitrate uptake might explain
why the rate of root respiration does not necessarily increase in proportion with the
increase in nitrate uptake (Granato et al., 1989).
Specific maintenance costs may also vary, but when grown with free access to all
nutrients, the total maintenance costs appear to be small compared with those for growth
15
and ion uptake (Fig. 7). Moreover, current evidence suggests that the specific costs for
maintenance respiration of the roots of slow-growing species are very similar to those of
inherently fast-growing species and thus cannot explain the relatively high rates of root
respiration of the slow-growing species (Scheurwater et al., 1998). One possibility is
that the specific maintenance costs increase with decreasing N supply (Van der Werf et
al., 1994); they may also become substantial in older plants, in which growth and the
rate of ion uptake has slowed down (Van der Werf et al., 1988).
Protein turnover is probably a major process contributing to maintenance respiration (De
Visser et al., 1992). So far the only roots for which protein half life values have been
published are those of the fast-growing Dactylis glomerata L. and of the slow-growing
Festuca ovina L., both grown at an optimum nutrient supply (Van der Werf et al.,
1992b; Scheurwater et al., 2000). These half-life values vary between 5 and 10 days.
Assuming biosynthetic costs of 15 mol ATP per mol peptide bond (Van der Werf et al.,
1994), only 15 to 30 nmol ATP g-1 s-1 are needed for the maintenance of the protein
pool. These costs account for less than half of the total maintenance respiration,
depending on the degradation constant used (Van der Werf et al., 1992a; 1992b). The
energy costs associated with maintaining ion gradients across root membranes may
represent a substantial portion of the remaining energy requirements of maintenance..
Bouma and De Visser (1993) calculated that it may account for most of the roots’
maintenance requirements.
Table 7 summarizes the information on specific respiratory energy costs for growth, ion
uptake and maintenance of root biomass, obtained with the methods illustrated in Fig.
6a, a closely related method (Veen, 1980), or a method which separates only two
components of respiration. The latter method yields values for maintenance respiration
and values for growth including ion uptake. It should be kept in mind that the present
method, as any other used so far in this area of research, is based on a number of
assumptions. Reasonable as these assumptions may appear, it should be stressed that no
experimental data are available to support that the specific costs for maintenance and
anion uptake do not vary with age. If they do, they will bias the results in a manner that
is not quite predictable.
VI. THE CAPACITY OF THE ALTERNATIVE PATH, ITS CONTRIBUTION TO
RESPIRATION AND ITS POSSIBLE SIGNIFICANCE IN THE FUNCTIONING
OF ROOTS
A. Assessment of alternative path activity
The capacity of the alternative path has been defined as the fraction of respiration that
proceeds in the presence of an inhibitor which fully blocks the cytochrome path and
which is sensitive to an inhibitor of the alternative path. (There is at least one exception
where the capacity of the alternative path cannot be determined in this manner. That is,
when the capacity of the alternative path exceeds the rate proceeding in the presence of
16
an inhibitor of the cytochrome path. In practice it means that there must be some
inhibition of respiration by an inhibitor of the cytochrome path to assess the capacity of
the alternative path). Only if the cytochrome path were fully saturated, could both the
capacity and the activity of the alternative path be assessed using the specific inhibitors
of the alternative and cytochrome pathways. However, the cytochrome path is probably
never saturated in vivo, since the control coefficient of the cytochrome path to overall
flux is quite low (Van den Bergen et al., 1994; Millar et al., 1995). As a result,
noninvasive measurements of alternative pathway respiration, using the 18O-isotope
fractionation method should be used (Guy et al., 1989; 1992; Henry et al. 1999).
The fact that SHAM additions can result in under-estimates of actual alternative
pathway activity (see section IV.A.1) means that previous measurements of alternative
and cytochrome pathway activity must be treated with great caution. The previous
studies do, however, demonstrate that the degree of SHAM inhibition and KCN-
resistance do vary between species and treatments. This suggests that differences in
alternative and cytochrome pathway activity do occur. Given the low number of
noninvasive studies that assess the level of alternative pathway respiration, we must at
present rely on the SHAM and KCN results to get some insight into what variations in
alternative and cytochrome pathway respiration occur. The following sections therefore
present the results of those inhibitor studies. The reader is advised to treat these studies
as an indicator of what levels of alternative pathway respiration occur in response to
environmental conditions, rather than the changes that do occur.
B. The physiological significance of the alternative path
In the short term, inhibition of respiration by SHAM decreases with decreasing
carbohydrate concentration in the roots (Fig. 3). However, when plants are exposed to a
low light intensity for an extended period, SHAM inhibition of root respiration is the
same as in plants grown at a higher light intensity (see section VII.A.7). Upon lowering
the water potential in the root environment of Plantago coronopus L., the demand for
carbohydrates for osmotic adjustment increases, and sorbitol, a compatible solute,
accumulates. The amount of glucose required for sorbitol synthesis in the roots during
the first 12 h (6.6 µmol glucose per gram fresh mass) matches the amount saved in root
respiration by a temporary reduction in (SHAM-sensitive) root respiration (62 µmol
glucose per gram dry mass; Fig. 8). When osmotic adjustment is completed, the SHAM
sensitivity returns to the level before the water potential decreased.
The two examples cited above have been used to illustrate that the activity of the
alternative path in roots appears to decrease when the availability of carbohydrates for
respiration decreases. On the other hand, it supposedly increases when the demand for
carbohydrates for other processes decreases, so that more is left for respiration.
Considering that the interpretation of the results was based on inhibitor studies, no firm
conclusion is possible. In fact, in roots of Poa annua the alternative pathway activity
(assessed with the 18O-isotope fractionation technique) was constant for 4 days after the
transfer from high light and short nights to low light and long night (Fig 9). During this
period both the activity of the cytochrome pathway and rate of total respiration
17
decreased, coinciding with a decline in the soluble sugar concentration (Millenaar et al.,
2000a).
In addition to changes in the carbohydrate availability, changes in the requirement for
respiratory energy may also affect the SHAM sensitivity of root respiration. De Visser et
al. (1986) found a transient increase in SHAM sensitivity in Pisum sativum roots upon
addition of nitrate to 2-week-old, nitrogen-deprived plants. In older pea plants, whose
cytochrome path was no longer controlled by adenylates, an increased SHAM sensitivity
was found upon addition of nitrate. Variation in SHAM sensitivity of respiration is
transient and tends to be followed by further adjustments in the roots’ metabolism. The
transient changes in SHAM sensitivity suggest that the nonphosphorylating path may
play a role in coping with relatively rapid changes in the environment.
As postulated by Purvis and Shewfelt (1993) a possible general function of the
alternative pathway is to stabilize the reduction state of the ubiquinone pool, thereby
preventing the extra production of oxygen free radicals. The in vivo reduction state of
the ubiquinone pool can be stabilized by the alternative pathway (Millenaar et al., 1998).
Transgenic tobacco plants that have a lower AOX expression show an increased oxygen
free radical production (Maxwell et al., 1999). The function of the alternative pathway
seems to be the prevention of the formation of extra oxygen free radicals. However,
there is no full proof, since there is no publication where oxygen free radical production,
AOX activity, superoxide dismutase (SOD) activity as well as the reduction state of the
ubiquinone pool have been measured.
VII. EFFECTS OF ENVIRONMENTAL CONDITIONS
Any factor that affects the respiratory energy requirement or the balance between
carbohydrate supply and carbohydrate demand in the roots is bound to affect root
respiration. Both the rate of respiration and the partitioning of electrons between the
cytochrome path and the alternative path may be affected by such environmental
conditions. In the following section both biotic and abiotic environmental factors,
known to affect root respiration, are discussed. As mentioned earlier, SHAM additions
frequently result in under-estimates of actual alternative pathway activity (section VI.A).
The reader is, therefore, advised to treat the following studies as an indicator of what
changes in alternative pathway respiration may occur in response to environmental
conditions.
A. Abiotic factors
Most environmental effects on root respiration can be understood on the basis of the
regulation of respiration as discussed in IV.A. In the following sections we analyze
some pertinent effects of nutrient supply, adverse soil conditions, including salinity and
drought, temperature and light conditions.
18
1. Nutrient supply
The well documented rapid effect of ions on root respiration, coined ‘salt respiration’
(Lundegardh, 1946; 1955), is probably partly due to the increased demand for
respiratory energy for ion transport (De Visser et al., 1986). Part of it might be due also
to a replacement of osmotically active sugars by inorganic ions, leaving a large amount
of sugars to be respired.
A sudden increase of the uptake and assimilation of nitrogen can have a significant
effect on root respiration. For example, exposure of nitrogen-starved Triticum aestivum
seedlings (pre-grown on CaSO4) to nitrate results in a transient increase in root
respiration (Barneix et al., 1984). This may be due to the increased demand for ion
transport and nitrogen assimilation. Addition of ammonium to the CaSO4-grown roots
resulted in an even larger increase (200%) in total respiration (Barneix et al., 1984).
Exposure to nitrate can result in higher rates of oxygen consumption relative to plants
exposed to ammonium (Lambers et al., 1980; De Visser and Lambers, 1983), possibly
reflecting the greater demands for metabolic energy associated with nitrate uptake (Pate,
1983). However, in other cases, a decrease in oxygen consumption is reported
(Blacquière et al., 1987; Bloom et al., 1992; Atkin and Cummins, 1994; 1995). Bloom
et al. (1992) found that lower rates of respiration in nitrate-grown Hordeum vulgare
plants depend on the ability of the roots to reduce nitrate: exposure of ammonium-grown
plants to nitrate only results in a decreased oxygen consumption when the root has the
ability to induce nitrate reductase. No effect of nitrate treatment was observed in plants
deficient in nitrate reductase (Bloom et al., 1992). A rise in the RQ is also associated
with the induction of nitrate reductase activity in Hordeum vulgare (Willis and Yemm,
1955; Jessop and Fowler, 1977; Bloom et al., 1992). The reduction in oxygen
consumption, and rise in RQ of nitrate-treated roots (relative to ammonium) may be due
to competition for reductant by nitrate reductase (Reed and Hageman, 1977; Sawhney et
al., 1978; Oaks and Hirel, 1985; Bloom et al., 1992).
Under steady-state conditions, when all plants are growing at the same rate, the
respiration of Pisum sativum roots is the same with nitrate and with ammonium as the
growth-limiting source of N (De Visser and Lambers, 1983). Somewhat higher rates of
root respiration occur in Plantago lanceolata L. and P. major when grown with an
optimum supply of ammonium than when grown with nitrate (Blacquière et al., 1987).
When plants are grown at a low supply of nutrients, their rate of root respiration is lower
than that of plants well supplied with mineral nutrients (Kuiper, 1983; Van der Werf et
al., 1992a). Under phosphate deprivation, there is no effect on the rate of root respiration
of Phaseolus vulgaris (Rychter and Mikulska, 1990), which is distinctly different from
the situation under limitation of all nutrients. It appears that the capacity of the
cytochrome path is greatly reduced, as demonstrated by the much lower rate of
respiration in the presence of an uncoupler and SHAM under phosphate deprivation.
The decline in activity of the cytochrome path may be compensated by an increased
activity of the alternative path, as suggested by a relatively strong effect of SHAM in
vivo (Rychter and Mikulska, 1990). Further studies on isolated mitochondria revealed
19
that the activity of cytochrome oxidase was reduced in the roots of phosphate-deficient
bean plants (Rychter et al., 1992).
2. pH
Root respiration rates can be affected by soil pH. For example, Yan et al. (1992)
reported that root respiration rates of Zea mays and Vicia faba L. increase as nutrient
solution pH values decrease. Net H+ release by H+-ATPase activity is a basic necessity
for continued root growth, and limits root growth at very low, critical pH values (Van
Beusichem 1982; Schubert et al., 1990). One way of coping with excess H+ uptake is to
increase active H+ pumping by plasma-membrane ATPases: such a response will
increase the demand for ATP. Yan et al. (1992) suggested that the increased root
respiration in response to noncritical low pH values is the result of increased H+ ATPase
activity (Yan et al., 1992). Increased respiration rates can therefore allow plants to
maintain root growth at noncritical low pH values, by increasing the supply of ATP for
H+ pumping by plasma-membrane ATPases.
At very low, critical pH values (less than 3.5 and 4.1 for Zea mays and Vicia faba,
respectively), root growth, net H+ release and respiration rates decline (relative to rates
at pH 7.0; Yan et al., 1992). Limitations in H+ pumping do not appear to be responsible
for the limited net H+ release and root growth below the critical pH values. Rather, the
increased entry of H+ into the roots appears to be responsible (Yan et al., 1992). Such
increased uptake of H+ would tend to disturb cytosolic pH and ultimately root growth
(Gerendas et al., 1990). The decrease in root respiration at very low pH values might
therefore be the result of decreased demand for growth respiration and/or the direct
effects of low cytosolic pH on the respiratory pathways.
3. Aluminum
High concentrations of soluble aluminum also affect root respiration rates (Tan and
Keltjens, 1990a,b; Collier et al., 1993; De Lima and Copeland, 1994) in soils of low pH:
the solubility of aluminum increases with decreasing pH (Foy et al., 1978; Fageria et al.,
1988).
The effects of aluminum on root respiration depend on whether whole root systems or
root tips are considered. In intact whole roots, Collier et al. (1993) found an increase in
respiration in both aluminum-tolerant and sensitive cultivars of Triticum aestivum,
during growth in the presence of a wide range of aluminum concentrations (0-900 mmol
m-3). The increase is entirely due to an enhanced level of SHAM-resistant respiration.
The pattern of the changes in respiration is similar for the tolerant and the sensitive
cultivar, be it that the peak in respiration occurs at a lower aluminum concentration for
the sensitive cultivar (100 vs. 350 mmol m-3). At higher aluminum concentrations
respiration rates gradually decline again to the control rates. This coincides with effects
on growth, which is not affected until much higher aluminum concentrations in the
tolerant cultivar. A similar stimulation of root respiration has been observed for a
sensitive (Tan and Keltjens, 1990a) and a tolerant (Tan and Keltjens, 1990b) cultivar of
Sorghum bicolor L.. De Lima and Copeland (1994) found an inhibition of the
20
respiration of excised root tips of a sensitive cultivar of Triticum aestivum, even at 75
mmol m-3 aluminum. Initially (12 h after exposure) only SHAM-resistant respiration is
inhibited, whereas later also SHAM-sensitive respiration is reduced. Mitochondria
isolated from roots of exposed plants have a diminished oxidative capacity.
The data on whole root systems and those on root tips suggest that the latter are
inhibited more readily by aluminum. The increase in respiration of the intact roots,
suggests that root functioning in the presence of aluminum imposes a demand for
additional respiratory energy. These increased costs have little to do with the mechanism
explaining tolerance, i.e. excretion of chelating organic acids, since such excretion does
not occur to any major extent in the sensitive cultivar (Delhaize et al., 1993).
4. Heavy metals
Root respiration appears to be inhibited by lead. For example, Koeppe (1977) found that
respiration of Zea mays root tips decreases by up to 40% within three hours of exposure
to 20 mol m-3 lead. The degree of inhibition increased with the duration of exposure.
Concomitant with the decrease in respiration of the root tips was a decrease in the
energy charge of the treated tissue (Koeppe, 1977). The response of whole root systems
to lead is not clear (see section VII. A.3 for a comparison of root tips and whole root
systems). It is also not clear to what extent respiration of roots is affected by lead in
natural soils.
Exposure of mitochondria isolated from etiolated Zea mays seedlings (using succinate as
a substrate) to lead also results in a 80% decrease in respiration (Koeppe and Millar,
1970). The addition of inorganic phosphate reverses the lead-induced succinate
inhibition. Koeppe (1981) suggested that lead decreases oxidative phosphorylation.
Cadmium and zinc also appear to inhibit seedling mitochondrial respiration in a manner
similar to that of lead (Bittell et al., 1974).
5. Salinity and drought
The rate of root respiration of the salt-tolerant Plantago coronopus declines when the
plants are transferred from a nonsaline nutrient solution to one containing 50 mol m-3
NaCl (Fig. 8). Prolonged exposure to 50 mol m-3 NaCl, a concentration sufficiently low
not to affect growth, has no effect on the rate of root respiration or the engagement of
the alternative path (Blacquière and Lambers, 1981). This similarity in growth and
respiratory pattern under saline and nonsaline conditions suggests that for roots of P.
coronopus the respiratory costs to cope with this salinity level are negligible. Similar
results were obtained for other salt-tolerant species, e.g., Plantago maritima (Lambers,
1979). Root respiration of the salt-tolerant grey mangrove Avicennia marina (Forsk.) is
stimulated by moderate concentrations of NaCl, which stimulate growth, and inhibited
by higher concentrations, which are inhibitory for growth (Burchett et al., 1984). That is,
root respiration follows the pattern of growth.
Different patterns are found for species that do not tolerate high levels of salinity. Root
respiration of two Hordeum vulgare cultivars increased upon exposure to 10 mol m-3
21
NaCl or KCl (Bloom and Epstein, 1984). Exposure to a solution from which ions can be
accumulated may lead to the replacement of sugars by inorganic ions and thus cause
increased engagement of the alternative path. Alternatively, the increased respiration
might reflect the increased costs for ion transport. Williams et al. (1991) exposed half of
the roots of Hordeum distichum to a non-permeating solute (mannitol or sorbitol at -0.4
MPa). This leads to a rapid but transient increase in (11C- or 14C-labeled) carbon import
and O2 consumption of the exposed root half, without any effect on the other part of the
root system. The increased import of carbon may be the cause for the rise in respiration,
but it cannot be excluded that the causal relationship is actually the other way around.
The rise in respiration may be due to a rise in the engagement of the alternative path or
reflect the energy demand of osmotic adjustment. The respiration of those roots of the
salt-sensitive Opuntia ficus-indica which are exposed to 30 or 100 mol NaCl m-3
increases, compared to that of roots of the same plants growing without NaCl. Contrary
to the results with H. distichum, this is not a transient effect; it is associated with a
reduction in growth of the exposed roots (Gersani et al., 1993). The rate of root
respiration (expressed per g DM) of Lycopersicon esculentum (L.) Mill and L. pennellii
(Correll) D’Arcy exposed to 100 mol m-3 NaCl for 10 days, decreases by 10 and 15%,
respectively, in comparison with plants grown in a nonsaline root medium (Taleisnik,
1987). At this salinity level, growth of both species is reduced, which may offer an
explanation for the reduced respiration rate.
Exposure to a dry soil leads to a gradual decline in root respiration of Triticum aestivum,
predominantly of the SHAM sensitivity (Nicolas et al., 1985). The decline in respiration
correlates with the accumulation of organic solutes. The authors interpreted the data in
the same manner as those on the short-term exposure of Plantago coronopus to NaCl
(Fig. 8), i.e. accumulation of osmotic solutes reduces the availability of sugars. This
subsequently leads to less grist for the mill of the alternative path.
The difference in response when comparing different species is likely to be associated
with the extent to which growth is affected. Plants whose growth is unaffected by
salinity, show a transient decline in root respiration or no response at all. In contrast,
root respiration is either enhanced when growth is inhibited by salinity or declines
parallel to the inhibition of growth. The respiratory costs of functioning in a saline
environment for adapted species that accumulate NaCl are likely to be relatively small.
For salt-excluding glycophytes this conclusion may be quite different. Experimentation,
in the sense as illustrated in Fig. 7, may provide further insight.
6. Temperature
Root respiration increases as a function of temperature, with the degree of increase being
dependent on the temperature coefficient (Q10) of respiration. Q10 values range between
1.1 and 2.9. Differences in Q10 values occur in some plants experiencing contrasting
growth temperatures (e.g., Gifford, 1995; Fitter et al., 1998). Moreover, although the
Q10 of root respiration is constant over a broad range of temperatures in many studies
(e.g., Tjoelker et al., 1999b), several others have reported that the Q10 varies with
measurement temperature (e.g., Higgins & Spomer, 1976; Crawford & Palin, 1981;
Berry and Raison, 1981; Palta and Nobel, 1989). Clearly, substantial variability in the
22
temperature sensitivity of root respiration often occurs.
The rate of root respiration at any given measuring temperature may also depend on the
degree to which the roots have acclimated to the growth temperature. Acclimation of
respiration to the growth temperature results in homeostasis of respiration, such that
warm-acclimated and cold-acclimated plants display similar rates of respiration when
measured at their respective growth temperatures (Körner and Larcher, 1988; Atkin et
al., 2000). Acclimation of root respiration to temperature occurs in Plantago lanceolata
(Smakman and Hofstra, 1982) and Zostera marina L. (Zimmerman et al., 1989).
However, no acclimation occurs in roots of Picea glauca (Moench) Voss (Weger and
Guy, 1991), Picea engelmannii Parry (Sowell and Spomer, 1986) or Abies lasiocarpa
(Hook.) Nutt. (Sowell and Spomer, 1986). Similarly, while acclimation to changes in
growth temperature results in near perfect homeostasis in Citrus volkameriana in wet
soils, no acclimation occurs in roots of the same species growing in dry soils (Bryla et
al., 1997). In those species where no thermal acclimation takes place, root respiration
rates will depend entirely on ambient temperature, with low temperatures severely
restricting root metabolism (Weger and Guy, 1991).
In addition to the acclimation potential of total root respiration, acclimation may also
occur within partitioning of electrons between the cytochrome and alternative pathways.
For example, transfer of Plantago lanceolata roots from 21oC to 13oC initially resulted
in a transient decline in SHAM-resistant respiration and an increase in SHAM-sensitive
respiration (after 2 h of exposure; Smakman and Hofstra, 1982). Extended exposure to
13oC (greater than 2 h) resulted in recovery in SHAM-resistance to its original level
(Smakman and Hofstra, 1982). The response of SHAM-sensitive respiration to extended
13oC exposure was more complex, with it first declining to a very low level, and then
returning to its original 21oC rate within 24 h. Transfer from 13oC to 21oC causes similar
acclimation in SHAM-resistant/-sensitive respiration (Smakman and Hofstra, 1982).
Presumably, some adjustment to temperature at the level of energy-requiring processes
or of the mitochondria occurs in roots that exhibit acclimation of electron-transport
chain partitioning. Such mitochondrial adjustment occurs in callus-forming potato tuber
discs: when grown at 28 C, the total respiratory capacity and the cyanide-resistance of
isolated mitochondria is larger than when grown at 8oC (Hemrika-Wagner et al., 1982).
In contrast to the data on Plantago lanceolata, Weger and Guy (1991) did not find any
acclimation of root mitochondrial electron transport to the growth temperature for Picea
glauca. At any one temperature, SHAM-sensitive and SHAM-resistant respiration rates
were independent of the growth temperature (4, 11, or 18oC; Weger and Guy, 1991).
Thermal acclimation of root respiration, therefore, appears to depend on both species
and environment. The probable mechanisms that underlie differences in the degree of
acclimation (and Q10 values) are discussed in Atkin et al. (2000).
The concentration of AOX protein often increases after transfer to lower temperatures
(Vanlerberghe and McIntosh 1992; Gonzàlez-Meler et al., 1999). Also KCN-
insensitive, SHAM-sensitive respiration increases as found frequently (Vanlerberghe
and McIntosh, 1992, and references therein). However, in a chilling-sensitive maize
cultivar the activity of the alternative pathway (18O-isotope fractionation) was higher
23
during the recovery period than in a less chilling-sensitive cultivar (Ribas-Carbo et al.,
2000).
Some plant species that are characteristic of cold environments exhibit inherently higher
root respiration rates relative to species characteristic of warmer environments. For
example, Higgins and Spomer (1976) found that root respiration rates were inherently
higher in the alpine Geum rossii (R.Br.) Ser. than in the sub-alpine Geum trifolium L..
Similarly, alpine populations of Achillea millefolium Pursh had higher respiration rates
than populations from more subalpine habitats (Higgins and Spomer, 1976). Soil
temperature decreases with increasing elevation or latitude (Higgins and Spomer, 1976).
The differences between the alpine and subalpine plants were maintained even when all
plants were grown under identical conditions (cold and warm soils). Similarly, Sowell
and Spomer (1986) reported that high elevation populations of Picea engelmannii and
Abies lasiocarpa had inherently higher root respiration rates than populations collected
from warmer, lower elevations, regardless of the growth treatment or measuring
temperature. In contrast, Keller (1967, as cited by Sowell and Spomer, 1986) found no
consistent trend in root respiration rates of high and low elevation populations of those
two species. Although high altitude populations of Picea abies had inherently higher
respiration rates relative to low altitude populations, the opposite was observed in Larix
decidua Miller populations. Similarly, specific rates of root respiration were not higher
in alpine Poa species than lowland Poa species, when both groups of species were
grown under common, constant environment conditions (Atkin, Botman and Lambers
1996). Thus, the relationship between elevation (and thus soil temperature) and
respiration appears to be species dependent.
7. Light conditions
As illustrated in Fig. 3 the rate of root respiration and the SHAM sensitivity are low
when the carbohydrate concentration in the roots is low. However, as long as the nights
are not too long, the rate of O2 consumption tends to be constant throughout the entire
day, also when plants are grown at a relatively low light intensity (see section IV.C).
During growth at a low light intensity, the rate of root respiration of Plantago major is
30-50% lower than that of plants grown at a high light intensity (Kuiper and Smid,
1985). Similar results have been obtained for many other species (Lambers and
Posthumus, 1980; Poorter, 1991; Millenaar et al., 2000a). This lower respiration rate is
likely to be associated with the low metabolic activity of roots, when plants grow at a
low light intensity.
Four days after transfer of Poa annua plants from an environment of high light intensity
and short nights to one of a low light intensity and long nights, the sugar concentration
and total respiration decreased to 10 and 60%, respectively. During this low-light period,
the concentration and reduction state of the alternative oxidase protein did not change as
compared with that before the transfer (Fig 10). Also the activity of the alternative
oxidase did not change (Fig 9), despite the large decrease in sugar concentration.
(Millenaar et al., 2000a).
24
8. Partial pressures of O2 and CO2 in the rhizosphere
The partial pressures of both O2 and CO2 in the soil may differ vastly from those in
normal air, especially upon flooding. Under such conditions the partial pressure of O2
drops to very low levels and it is well documented that plants that occur naturally in
flooded soils have a well developed aerenchyma, allowing diffusion of O2 to the roots
(Jackson and Armstrong, 1999). Such an aerenchyma avoids inhibition of respiration
due to lack of O2, which is inevitable for plants that are not adapted to wet soils (Perata
and Alpi, 1993). CO2 partial pressures increase upon flooding of the soil. Nobel and
Palta (1989) found values of 2,400 and 4,170 µl CO2 l-1 (0.2 and 0.4%, respectively) in
flooded soils supporting the growth of desert succulents, as opposed to 540 and 1,080 µl
l-1 in the same soils, when well drained. Under flooded conditions, the O2 concentration
in these soils is virtually the same as that of well drained soils. Considerably lower O2
and higher CO2 concentrations have been found by other authors, depending both on soil
type and the metabolic activity of the plant cover. For example, Good and Patrick (1987)
found O2 concentrations as low as 1.2% and CO2 concentrations of 56 and 38% in silt
loam, supporting the growth of Fraxinus pennsylvanica Marsh. and Quercus nigra L.,
respectively. In the air spaces of these roots, CO2 concentrations of 10.4 (Fraxinus) and
15% (Quercus) were found.
Compared with the wealth of papers on the inhibition of leaf respiration by an elevated
CO2 concentration (700 vs. 350 µl CO2 l-1 in normal air; e.g., Drake et al., 1999), little
research has been done on effects of CO2 on root respiration. Nobel and Palta (1989)
found a reversible inhibition of root respiration by 5000 µl CO2 l-1 of 35 and 46% for the
cacti Opuntia ficus-indica (L.) Miller and Ferocactus acanthodes (Lemaire) Britton and
Rose, respectively. For both species, root respiration is fully inhibited by 20,000 µl CO2
l-1 (2%), which is an irreversible effect if lasting for 4 hours, leading to death of cortical
cells. Very similar effects were found for another desert succulent: Agave deserti Engel.
(Palta and Nobel, 1989). Death of the cortical cells is unlikely to be due to inhibition of
respiration, since exposure to a root atmosphere without O2 for a similar period is fully
reversible for the same plants.
The effects of CO2 on root respiration of desert succulents are possibly indirect, and due
to inhibition of energy-requiring processes. However, the effects may also in part be
direct, since Palet et al. (1991) and Gonzàlez -Meler et al. (1996) showed that the
activity of the cytochrome path is inhibited by CO2, apparently at the level of
cytochrome oxidase. Qi et al. (1994) and Burton (1997) also found inhibition of root
respiration by soil CO2 levels in a range normally found in soil for C3 plants
(Pseudotsuga menziessii and Acer saccharum, sugar maple), whereas no such inhibition
was found for a range of other species studied by other authors (e.g., Bouma et al.,
1997a,b; Scheurwater et al., 1998). Because respiration is only affected by CO2, and not
by bicarbonate (Palet et al., 1992), the pH of the root environment might affect
experimental results.
The information in the literature is too scanty to conclude that the effects observed for
25
desert succulents are valid for other plants also. However, long-term exposure to CO2
concentrations in the root gas phase as high as 10.4 and 15.0% allows growth of
Fraxinus pennsylvanica and Quercus nigra, respectively (Good and Patrick, 1987).
Also, growth of Avena sativa L. (Stolwijk and Thimann, 1957) and Nicotiana tabacum
L. (Williamson and Splinter, 1968) is relatively little affected by exposure to 6.5 and
18.5% CO2, respectively. Roots of other species (Pisum sativum, Phaseolus vulgaris
and Vicia faba; Stolwijk and Thimann, 1957) are more sensitive, e.g., cell division of
Vicia faba is inhibited as soon as the CO2 concentrations exceeds 6% (Williamson
1968) and the growth of Triticum aestivum L. is less when the roots are exposed to
aerobic conditions with 10% CO2 compared with an aerobic control (Trought and Drew,
1980). However, it appears that most species are considerably less sensitive to a high
CO2 concentration in the root environment than are desert succulents.
In the absence of further information, it would seem that root respiration of plants other
than desert succulents is not particularly sensitive to CO2. What then is so special about
the respiration of desert succulents? Do the investigated desert succculents, all of which
are CAM plants, perhaps have a large capacity for net CO2 fixation via PEP-carboxylase
in their roots? Hew (1976) provided evidence for CO2 fixation by aerial roots of tropical
orchids, showing CAM metabolism in their thick leaves. CO2 assimilation is only
apparent during the day, suggesting that it may not be mediated by PEP carboxylase and
lead to malic acid production. To our knowledge, there is no information available on
the significance of net dark CO2 fixation in non-aerial roots of CAM plants, other than
that which normally occurs in all roots to provide the major substrate for the
mitochondria (Bryce and ap Rees, 1985b). If net dark CO2 fixation via PEP carboxylase
does occur, it might lead to a rapid accumulation of malic acid beyond what can be
stored in vacuoles or exported via the xylem. This might lead to acidification of the
cytosol and be the cause of the death of cortical cells (Nobel and Palta, 1989). The lack
of such presumed capacity for net CO2 fixation in non-CAM plants might account for
their relatively low sensitivity to the CO2 concentration in the rhizosphere; however, so
far this is mere speculation.
B. Biotic factors
1. Effects of symbiotic organisms
Carbon costs of N-assimilation of legumes have been extensively studied by Pate and
coworkers (e.g., Pate et al., 1979). The costs of N2-fixation are invariably higher than
those of nitrate assimilation (Table 2). Ryle and coworkers made a more detailed
analysis of the respiratory costs of N2-fixation. When the oxygen concentration
surrounding nodulated roots is lowered to 3%, which is sufficiently low to completely
stop the respiration of the nodules but high enough for that of the roots to proceed, the
production of carbon dioxide declines to about 30% of the control roots (Ryle et al.,
1984). Using this approach, the respiration of roots has been separated from that of
nodules. For Glycine max, completely dependent on the symbiont Rhizobium for its
nitrogen supply, the specific respiration rate of the nodules is almost 5 times higher than
that of the roots (Ryle et al., 1984). The average respiratory costs of N-assimilation in
26
these nodulated roots is 13.2 mg CO2 (mg N)-1, of which 80% is associated with the
activity of nitrogenase and ammonium assimilation and the rest with growth and
maintenance of nodules.
Assuming a respiratory quotient of 1.4 (De Visser, 1985) and an ADP:O ratio of 3
(which is a likely value, since the alternative path does not contribute to respiration in
infected cells of nodules; Kearns et al., 1992), the cost can be expressed in the same
units as for the uptake of ions (Table 7). Since nitrate is the major anion taken up, the
main part of the respiratory energy for anion uptake is for the absorption of nitrate. In
addition, the values presented in Table 7 may include some costs for synthesis of amino
acids to be translocated to the shoot and for transport of nitrogenous compounds to the
shoot (Van der Werf et al., 1988). A valid comparison with the values for anion uptake
and the costs for symbiotic fixation of nitrogen and associated costs is thus possible. The
cost for the symbiotic system is 18 mol ATP (mol N)-1. A comparison with the data on
the cost of a non-symbiotic system using nitrate shows that the assimilation of
atmospheric nitrogen in symbiosis with Rhizobium is a costly process. This explains
why the respiration of nodulated roots of Trifolium repens L. is largely associated with
the process of nitrogen fixation (Ryle et al., 1985a). Expressed in the units used in Table
2: In T. repens N2-fixation requires 23% of the photosynthates produced daily (Ryle et
al., 1985b).
The legume-Rhizobium symbiosis has been studied more intensively than other systems,
e.g., where cyanobacteria or actinomycetes are the N2-fixing symbionts. Some work has
been done on the Alnus rubra-Frankia system (Tjepkema and Winship, 1980; Winship
and Tjepkema, 1982) and the Cycas circinalis-Nostoc system (Tredici et al., 1988).
The carbon costs of another symbiotic system, that between higher plants and
mycorrhizal fungi, has been given less attention. Mycorrhizal roots of Vicia faba (Pang
and Paul, 1980), Allium porrum (Snellgrove et al., 1982), Glycine max (Harris et al.,
1985), Plantago major (Baas et al., 1989) and Citrus volkameriana Tan. & Pasq. (Peng
et al., 1993) have a higher rate of respiration than nonmycorrhizal ones. However, the
rate of root respiration of mycorrhizal and nonmycorrhizal Trifolium subterraneum L.
plants is the same (Silsbury et al., 1983).
The costs of the mycorrhizal symbiosis have been estimated in different ways, e.g., by
comparing the translocation of 14C assimilates to the mycorrhizal and the
nonmycorrhizal half of a split-root system (Koch and Johnson, 1984; Douds et al.,
1988), by measuring the flow of 14C labeled assimilates into soil and external hyphae
(Jakobsen and Rosendahl, 1990), and by comparing the rate of root respiration of
nonmycorrhizal with that of mycorrhizal plants growing at the same rate (Snellgrove et
al., 1982, Baas et al., 1989). The estimates vary between 4 and 20% of the carbon fixed
in photosynthesis. However, symbiotic plants tend to have a higher rate of
photosynthesis per plant, partly due to their greater leaf area. Therefore, as long as
phosphate is limiting, mycorrhizal plants usually grow faster, despite the large carbon
sink of the symbiotic system.
Baas et al. (1989) further investigated the increase in root respiration in Plantago major
27
L. ssp. pleiosperma (Pilger) infected with the vesicular-arbuscular mycorrhizal fungus
Glomus fasciculatum (Thaxt. sensu Gerdemann) Gerdemann and Trappe. In comparison
with nonmycorrhizal plants growing at the same rate, the estimated rate of ATP
production in root respiration is increased by 80% (Fig. 11). Since mycorrhizal P. major
plants absorb more ions from the substrate than the nonmycorrhizal ones, Baas and
coworkers analyzed whether the increased respiration could be explained by the
increased energy demand for ion uptake. They concluded that only a minor part (15%)
of the increased rate of ATP production is associated with an increased rate of ion
uptake by the mycorrhizal roots. The major part (83%) is explained by the respiratory
metabolism of the fungus and/or other effects of the fungus on the roots’ metabolism.
Construction costs of fibrous roots are also higher for mycorrhizal than for
nonmycorrhizal roots due to their higher fatty acid concentration (Peng et al., 1993).
2. Effects of parasitic organisms
Root respiration of both Brassica campestris L. and Lycopersicon esculentum is
approximately 50% higher in plants infected by the angiosperm parasite Orobanche
aegyptica Pers. or O. cernua Loefll. than in control plants (Singh and Singh, 1971). The
respiration is increased most near the point of infection.
Tap roots of Beta vulgaris plants, infected with Beta Virus 4, also respire more than
uninfested plants, except when stored at a rather cool temperature of 2oC (Löhr and
Müller, 1952). Infection of Ipomoea batatas Lam. root tissue slices by the parasitic
fungus Ceratocystis fimbriata Ellis & Halst. ex. Ipomoea batatas (14137 C.F. Andrus)
induces a four-fold increase in the rate of respiration in 40 h (Uritani and Asahi, 1980).
The pattern of the increase in respiration is biphasic. The first phase, reaching a
maximum after 20 h, occurs also in wounded tissue. It is probably associated with the
normal wound response and presumably due to an increased energy demand for the
synthesis of cell walls and other compounds. The second phase is more specifically
associated with the infection and may be caused by the increased energy demand for the
production of various metabolites (e.g., phytoalexins), whose synthesis is induced upon
infection. In leaves, an increase in respiration upon infection with powdery mildew
appears to be associated with an increase in activity of both the cytochrome and the
alternative path (Farrar, 1992).
Upon attack by pathogens, energy-requiring processes tend to increase. Infection of
roots of a susceptible variety of Lycopersicon esculentum by the nematode Meloidogyne
incognita, race 2, Kofoid and White, root respiration first increases but returns to the
level of uninfested plants 8 days after inoculation (Zacheo and Molinari, 1987). A
resistant variety responds in exactly the opposite way: at first there is no effect on root
respiration, but after 8 days the rate exceeds that of control plants. The initial increase in
the susceptible plants is associated with an increased SHAM sensitivity, whereas the
much slower response in the resistant plants is not. Further studies using the oxygen
isotope-fractionation technique are required before any conclusion can be reached on the
contribution of the alternative path in the observed changes in respiration.
28
VIII. CONCLUDING REMARKS
In the last decade our understanding of the regulation of root respiration and of the
carbon costs of the various processes in roots of higher plants has increased
considerably. Some specific areas need further development. In view of recent
developments on the biochemical regulation of the alternative oxidase in isolated
mitochondria, the control of the activity of the alternative path in intact roots deserves
further attention. Our understanding of the specific respiratory cost that is associated
with ion uptake in fast- and slow-growing species has increased substantially. However,
we still have no information on the biochemical basis of the likely environmentally-
induced variation in the specific costs of ion transport. A full understanding of the
survival value of the nonphosphorylating, alternative pathway, which may affect the
carbon costs of the roots’ functioning to a major extent, is still lacking. Further
development is to be expected from investigations of genetically modified plants which
lack alternative path capacity, due to a transformation using antisense DNA
(Vanlerberghe et al., 1994).
The fraction of carbon produced in photosynthesis that is subsequently utilized in the
growth and respiration of roots and their symbionts is certainly of major quantitative
importance. Recent developments that are described in the present chapter have
uncovered some of the carbon costs of ‘the hidden half’. This information may prove
useful in future modeling of plant growth and has already helped us to understand
optimum patterns of investment in relation to environmental conditions (Van der Werf
et al., 1993). Only too often such models incorporate intricate details of the production
of carbon in photosynthesis, whilst only including ballpark estimates of the consumption
of carbon for growth and respiration in roots. Since information compiled in this chapter
demonstrates that there is no fixed ratio between the utilization of carbon for root
growth and that for root respiration, more detailed information may have to be included
in models referred to above. Such information is now widely available for a range of
species.
REFERENCES
Agius, S.C., Bykova, N.V., Igamberdiev, A.U., and Møller, I.M. (1998). The
internal rotenone-insensitive NADPH dehydrogenase contributes to malate
oxidation by potato tuber and pea leaf mitochondria. Physiol. Plant. 104:
329-336.
Atkin, O.K., Villar, R., and Lambers, H. 1995. Partitioning of electrons between the
cytochrome and the alternative pathways in intact roots. Its implications for the ATP-
yield in vivo. Plant Physiol. 108: 1179-1183.
Atkin, O.K., Botman, B., and Lambers, H. 1996. The causes of inherently slow growth
in alpine plants: an analysis based on the underlying carbon economies of alpine and
lowland Poa species. Funct. Ecol. 10: 698-700.
29
Atkin, O.K., Edwards, E.J., and Loveys, B.R (2000). Response of root respiration to
changes in temperature and its relevance to global warming. New Phytol. 147: 141-
154.
Atkinson, C.J. and Farrar, J.F. 1983. Allocation of photosynthetically fixed carbon in
Festuca ovina L. and Nardus stricta L. New Phytol. 95: 519-531.
Baas, R., Van der Werf, A., and Lambers, H. 1989. Analysis of growth and root
respiration in Plantago major ssp. pleiosperma: effects of VA mycorrhizal infection and
P addition. Plant Physiol. 91: 227-232.
Bahr, J.T. and Bonner, W.D., Jr. 1973a. Cyanide-insensitive respiration. I. The steady
states of skunk cabbage spadix and bean hypocotyl mitochondria. J. Biol. Chem. 248:
3441-3445.
Bahr, J.T. and Bonner, W.D., Jr. 1973b. Cyanide-insensitive respiration. II. Control of
the alternative pathway. J. Biol. Chem. 248: 3446-3450.
Barneix, A.J., Breteler, H., and Van de Geijn, S.C. 1984. Gas and ion exchanges in
wheat roots after nitrogen supply. Physiol. Plant. 61: 357-362.
Ben Zioni, A., Vaadia, Y., and Lips, S.H. 1971. Nitrate uptake by roots as regulated by
nitrate reduction products of the shoot. Physiol. Plant. 24: 288-290.
Berry, L.J. 1946. The influence of oxygen tension on the respiratory rate in different
segments of onion roots. J. Cell. Comp. Physiol. 33: 41-66.
Berry, L.J. and Brock, M.J. 1946. Polar distribution of respiratory rate in the onion root
tip. Plant Physiol. 21: 542-549.
Berry, J.A. and Raison, J.K. 1981. Responses of macrophytes to temperature. In:
Lange OL, Nobel PS, Osmond CB, Zeigler H, eds. Physiological Plant Ecology I.
Responses to the Physical Environment. Springer-Verlag, Berlin, 277-338.
Bingham, I.J. and Farrar, J.F. 1987. Respiration of barley roots: Assessment of activity
of the alternative path using SHAM. Physiol. Plant. 70: 491-498.
Bingham, I.J. and Farrar, J.F. 1988. Regulation of respiration in barley roots. Physiol.
Plant. 73: 278-285.
Bittell, J.E., Koeppe, D.E., and Millar, R.J. 1974. Sorption of heavy metal cations by
corn mitochondria and the effects on electron and energy transfer reactions. Physiol.
Plant. 30: 226-230.
Blacquière, T. 1987. Ammonium nutrition in Plantago lanceolata L. and P. major L.
ssp. major. II. Efficiency of root respiration and growth. Comparison of measured and
30
theoretical values of growth respiration. Plant Physiol. Biochem. 25: 775-785.
Blacquière, T. and Lambers, H. 1981. Growth, photosynthesis and respiration in
Plantago coronopus as affected by salinity. Physiol. Plant. 51: 265-268.
Blacquière, T., Hofstra, R., and Stulen, I. 1987. Ammonium and nitrate nutrition in
Plantago lanceolata and Plantago major L. I. Aspects of growth, chemical composition
and root respiration. Plant Soil 104: 129-141.
Bloom, A. and Epstein, E. 1984. Varietal differences in salt-induced respiration in
barley. Plant Sci. Lett. 35: 1-3.
Bloom, A.J., Sukrapanna, S.S., and Warner, R.L. 1992. Root respiration associated with
ammonium and nitrate absorption and assimilation by barley. Plant Physiol. 99: 1294-
1301.
Boot, R.G.A., Schildwacht, P.M., and Lambers, H. 1992. Partitioning of nitrogen and
biomass at a range of N-addition rates and their consequences for growth and gas
exchange in two perennial grasses from inland dunes. Physiol. Plant. 86: 152-160.
Bouma, T.J. (1995) Utilization of respiratory energy in higher plants. Requirements for
‘maintenance’ and transport processes. PhD Thesis, Wageningen Agricultural
University.
Bouma, T.J. and De Visser, R. 1993. Energy requirements for maintenance of ion
concentrations in roots. Physiol. Plant. 89: 133-142.
Bouma, T., Nielsen, K.L., Eissenstat, D.M., and Lynch, J.P. (1997a) Estimating
respiration of roots in soil: interactions with soil CO2, soil temperature and soil water
content. Plant Soil 195: 221-232.
Bouma, T., Nielsen, K.L., Eissenstat, D.M., & Lynch, J.P. (1997b) Soil CO2
concentration dos not affect growth or root respiration in bean and citrus. Plant, Cell
Environ. 20: 1495-1505.
Bowling, D.J.F. 1981. Evidence for an ion uptake controller in Helianthus annuus. In
Structure and Function of Plant Roots (R. Brouwer, O. Gasparikova, J. Kolek, and B.G.
Loughman, Eds.). Martinus Nijhoff/Dr W. Junk Publishers, The Hague, pp. 179-186.
Brambilla, I., Bertani, A., and Reggiani, R. 1986. Effect of inorganic nitrogen nutrition
(ammonium and nitrate) on aerobic metabolism in excised rice roots. J. Plant Physiol.
123: 419-428.
Brouquisse, R., James, F., Raymond, P., and Pradet, A. 1991. Study of glucose
starvation in excised maize root tips. Plant Physiol. 96: 619-626.
31
Bryce, J.H. and ap Rees, T. 1985a. Effects of sucrose on the rate of respiration of the
roots of Pisum sativum. J. Plant Physiol. 120: 363-367.
Bryce, J.H. and ap Rees, T. 1985b. Rapid decarboxylation of the products of dark
fixation of CO2 in roots of Pisum and Plantago. Phytochemistry 24: 1635-1638.
Burchett, M.D., Field, C.D., and Pulkownik, A. 1984. Salinity, growth and root
respiration in the grey mangrove, Avicennia marina. Physiol. Plant. 60: 113-118.
Burton, A.J., Zogg, G.P., Pregitzer, K.S., & Zak, D.R. (1997) Effect of measurement
CO2 concentration on sugar maple root respiration. Tree Physiol. 17: 421-427.
Casadesus, J., Tapia, L. & Lambers, H. 1995. Regulation of K+ and NO3- fluxes in roots
of sunflower (Helianthus annuus L.) after changes in light intensity. Physiol. Plant. 93:
279-285.
Challa, H. 1976. An analysis of the diurnal course of growth, carbon dioxide exchange
and carbohydrate reserve content of cucumber. Agricultural Research Reports 861,
Centre for Agricultural Publishing and Documentation, Wageningen.
Christofferson, R.E., and Laties, G.G. 1982. Ethylene regulation of gene expression in
carrots. Proc. Natl. Acad. Sci. USA 79: 4060-4063.
Collier, D.E., Ackermann, F., Somers, D.J., Cummins, W.R., and Atkin, O.K. 1993. The
effect of aluminium exposure on root respiration in an aluminium-sensitive and an
aluminium-tolerant cultivar of Triticum aestivum. Physiol. Plant. 87: 447-452.
Crawford, R.M.M. and Palin, M.A. 1981. Root respiration and temperature limits to the
north-south distribution of four perennial maritime plants. Flora 171: 338-354.
Curran, M., Cole, M., Allaway, W.G. 1986. Root aeration and respiration in young
mangrove plants (Avicennia marina (Forsk.) Vierh.). J. Exp. Bot. 37: 1225-1233.
Day, D.A. and Lambers, H. 1983. The regulation of glycolysis and electron transport in
roots. Physiol. Plant. 58: 155-160.
Day, D.A., Millar, A.H., Wiskich, J.T., and Whelan, J. 1994. Regulation of alternative
oxidase activity by pyruvate in soybean mitochondria. Plant Physiol. 106: 1421-1427.
Day, D. A., Krab, K., Lambers, H., Moore, A. L., Siedow, J. N., Wagner, A. M. and
Wiskich, J. T. (1996). The cyanide-resistant oxidase: To inhibit or not to inhibit,
that is the question. Plant Physiol. 110: 1-2.
Delhaize, E., Ryan, P.R., and Randall, P.J. 1993. Aluminium tolerance in wheat
(Triticum aestivum L.). II. Aluminium-stimulated excretion of malic acid from root
32
apices. Plant Physiol. 103: 695-702.
De Lima, M.L. and Copeland, L. 1994. The effect of aluminium on respiration of wheat
roots. Physiol. Plant. 90: 51-58.
De Visser, R. 1985. Efficiency of respiration and energy requirements of N assimilation
in roots of Pisum sativum. Physiol. Plant. 65: 209-218.
De Visser, R. and Blacquière, T. 1984. Inhibition and stimulation of root respiration in
Pisum and Plantago by hydroxamate. Its consequences for the assessment of alternative
path activity. Plant Physiol. 75: 813-817.
De Visser, R. and Lambers, H. 1983. Growth and the efficiency of root respiration of
Pisum sativum as dependent on the source of nitrogen. Physiol. Plant. 58: 533-543.
De Visser, R., Spreen Brouwer, K., and Posthumus, F. 1986. Alternative path mediated
ATP synthesis in roots of Pisum sativum upon nitrogen supply. Plant Physiol. 80:
295-300.
De Visser, R., Spitters, C.T.J., and Bouma, T.J. 1992. Energy costs of protein turnover:
Theoretical and experimental estimation from regression of respiration on protein
concentration of full-grown leaves. In Molecular, Biochemical and Physiological
Aspects of Plant Respiration (H. Lambers, and L.H.W. Van der Plas, Eds.). SPB
Academic Publishing, The Hague, pp. 493-508.
Dizengremel. P., Chauveau, M., and Roussaux, J. 1982. Inhibition by adenine
derivatives of the cyanide-insensitive electron transport pathway of plant mitochondria.
Plant Physiol. 70: 585-589.
Douds, D.D., Johnson, C.R., and Koch, K.E. 1988. Carbon cost of the fungal symbiont
relative to net leaf P accumulation in a split-root VA mycorrhizal symbiosis. Plant
Physiol. 86: 491-496.
Drake, B.G., Azcón-Bieto, J., Berry, J., Bunce, J., Dijkstra, P., Farrar, J., Gifford,
R.M., Gonzàlez-Meler, M.A., Koch, G., Lambers, H., Siedow, J., and Wullschleger,
S. 1999. Does elevated atmospheric CO2 concentration inhibit mitochondrial
respiration in green plants? Plant, Cell Environ. 22: 649-657.
Dry, I.B., Moore, A.L., Day, D.A., and Wiskich, J.T. 1989. Regulation of alternative
pathway activity in plant mitochondria. Non-linear relationship between electron flux
and the redox poise of the quinone pool. Arch. Biochem. Biophys. 273: 148-157.
Duarte, P., Larsson, C.-M., and Tilberg, J.E. 1988. Carbon and nitrate utilization in
shoots and roots of nitrogen-limited Pisum. In Structural and Functional Aspects of
Transport in Roots (B. Loughman, O. Gasparikova, and J. Kolek, Eds.). Kluwer
Academic Publishers, Dordrecht. pp. 199-202.
33
Fageria, N.K., Baligar, V.C., and Wright, R.J. 1988. Aluminium toxicity in crop plants.
J. Plant Nut. 11: 303-319.
Farrar, J.F. 1981. Respiration rate of barley roots: Its relation to growth, substrate supply
and the illumination of the shoot. Ann. Bot. 48: 53-63.
Farrar, J.F. 1985. Fluxes of carbon in roots of barley plants. New Phytol. 99: 57-69.
Farrar, J.F. 1992. Beyond photosynthesis: the translocation and respiration of diseased
leaves. In Pests and Pathogens (P.G. Ayres, Ed.). Bios Scientific Publishers, Oxford, pp.
107-127.
Farrar, J.F. and Jones, C.L. 1986. Modification of respiration and carbohydrate status of
barley roots by selective pruning. New Phytol. 102: 513-521.
Fitter A.H., Graves, J.D., Self, G.K., Brown, T.K., Bogie, D.S., and Taylor, K. 1998.
Root production, turnover and respiration under two grassland types along an
altitudinal gradient - influence of temperature and solar radiation. Oecologia 114: 20-
30.
Foy, C.D., Chaney, R.L., and White, M.C. 1978. The physiology of metal toxicity in
plants. Annu. Rev. Plant Physiol. 29: 511-566.
Gärdenäs, A.I. 2000. Soil respiration fluxes measured along a hydrological gradient in a
Norway spruce stands in South Sweden (Skogaby). Plant Soil, in press
Gerendas, J., Ratcliffe, R.G., and Sattelmacher, B. 1990. 31P nuclear magnetic resonance
evidence for differences in intracellular pH in the roots of maize seedlings grown with
nitrate or ammonium. J. Plant Physiol. 137: 125-128.
Gersani, M., Graham, E.A., and Nobel, P.S. 1993. Growth responses of individual roots
of Opuntia ficus-indica to salinity. Plant Cell Environ. 16: 827-834.
Gifford, R.M. 1995. Whole plant respiration and photosynthesis of wheat under
increased CO2 concentration and temperature - long-term versus short-term
distinctions for modelling. Global Change Biol. 1: 385-396
Goddard, D.R. and Bonner, W.D. 1960. Cellular Respiration. In Plant Physiology, A
Treatise, Vol. IA. (F.C. Steward, Ed.). Academic Press, New York, pp. 209-312.
Gonzàlez -Meler, M.A., Ribas-Carbo, M., Siedow, J.N., and Drake, B.G. 1996. Direct
inhibition of plant mitochondrial respiration by elevated CO2. Plant Physiol. 112:
1349-1355.
Gonzàlez-Meler, Ribas-Carbo, M., Giles, L., and Siedow, J.N. 1999. The effect of
growth and measurement temperature on the activity of the alternative respiratory
pathway. Plant Physiol. 120: 765-772.
34
Good, B.J. and Patrick, W.H. 1987. Gas composition and respiration of water oak
(Quercus nigra L.) and green ash (Fraxinus pennsylvanica Marsh.) roots after prolonged
flooding. Plant Soil 97: 419-427.
Granato, T.C., Raper, C.D. Jr., and Wilkerson, G.G. 1989. Respiration rate in maize
roots is related to concentration of reduced nitrogen and proliferation of lateral roots.
Physiol. Plant. 76: 419-424.
Greenway, H. and West, K.R. 1973. Respiration and mitochondrial activity in Zea mays
roots as affected by osmotic stress. Ann. Bot. 37: 21-35.
Guy, R.D., Berry, J.A., Fogel, M.L., and Hoering, T.C. 1989. Differential fractionation
of oxygen isotopes by cyanide-resistant and cyanide-sensitive respiration in plants.
Planta 177: 483-491.
Guy, R.D., Berry, J.A., Fogel, M.L., Turpin, D.H., and Weger, H.G. 1992. Fractionation
of the stable isotopes of oxygen during respiration by plants - the basis of a new
technique to estimate partitioning to the alternative path. In Plant Respiration.
Molecular, Biochemical and Physiological Aspects (H. Lambers, and L.H.W. Van der
Plas, Eds.). SPB Academic Publishing, The Hague, pp. 443-453.
Hansen, G.K. 1980. Diurnal variation of root respiration rates and nitrate uptake as
influenced by nitrogen supply. Physiol. Plant. 48: 421-427.
Hansen, G.K. and Jensen, C.R. 1979. Growth and maintenance respiration in whole
plants, tops and roots of Lolium multiflorum. Physiol. Plant. 39: 155-164.
Harris, D., Pacovsky, R.S., and Paul, E.A. 1985. Carbon economy of soybean-
Rhizobium-Glomus associations. New Phytol. 101: 427-440.
Hatrick, A.A. and Bowling, D.J.F. 1973. A study of the relationship between root and
shoot metabolism. J. Exp. Bot. 24: 607-613.
Hemrika-Wagner, A.M., Kreuk, K.C.M., and Van der Plas, L.H.W. 1982. Influence of
growth temperature on respiratory characteristics of mitochondria from callus-forming
potato tuber discs. Plant Physiol. 70: 602-605.
Henry, B.K., Atkin, O.K., Day, D.A., Millar, A.H., Menz, R.I. and Farquhar, G.D.
1999. The oxygen isotope discrimination technique for studying plant respiration:
assessing sources of variability in its application. Aust J Plant Physiol 26: 773-780.
Hew, C.-S. 1976. Patterns of CO2 fixation in tropical orchids species. Proceedings 8th
World Orchid Conference, pp. 426-430.
Higgins, P.D. and Spomer, G.G. 1976. Soil temperature effects on root respiration and
the ecology of alpine and subalpine plants. Bot. Gaz. 137: 110-120.
35
Hoefnagel, M.H.N., Millar, A.H., Wiskich, J.T., and Day, D.A. (1995) Cytochrome and
alternative respiratory pathways compete for electrons in the presence of pyruvate in
soybean mitochondria. Arch. Biochem. Biophys. 318: 394-400.
Huck, M.G., Hageman, R.H., and Hanson, J.B. 1962. Diurnal variation in root
respiration. Plant Physiol. 37: 371-375.
Imsande, J. and Touraine, B. 1994. N demand and the regulation on nitrate uptake. Plant
Physiol. 105: 3-7.
Jackson, M.B. and Armstrong, W. 1999. Formation of aerenchyma and the processes of
plant ventilation in relation to soil flooding and submergence. Plant Biol. 1: 274-287.
Jakobsen, I. and Rosendahl, L. 1990. Carbon flow into soil and external hyphae from
roots of mycorrhizal cucumber plants. New Phytol. 115: 77-83.
Johansson, G. 1991. Carbon distribution in meadow fescue (Festuca pratensis L.)
determined in a growth chamber with 14C-labelled atmosphere. Acta Agric. Scand. 41:
37-46.
Johansson, G. 1992. Below-ground carbon distribution in barley (Hordeum vulgare L.)
with and without nitrogen fertilization. Plant Soil 144: 93-99.
Kandler, O. 1953. Ueber den ‘synthetischen Wirkungsgrad’ in vitro kultivierter
Embryonen, Wurzeln und Spross. Z. Naturforsch. 8B: 109-117.
Karlsson, B. and Eliasson, L. 1955. The respiratory quotient in different parts of wheat
root in relation to growth. Physiol. Plant. 8: 561-571.
Kearns, A., Whelan, J., Young, S., Elthon, T.E., and Day, D.A. 1992. Tissue-specific
expression of the alternative oxidase in soybean and siratro. Plant Physiol. 99: 712-717.
Koch, K.E. and Johnson, C.R. 1984. Photosynthate partitioning in split-root citrus
seedlings with mycorrhizal and non-mycorrhizal root systems. Plant Physiol. 75: 26-30.
Koeppe, D.E. 1977. The uptake, distribution, and effect of cadmium and lead in plants.
Sci. Tot. Environ. 7: 197-206.
Koeppe, D.E. 1981. Lead: Understanding the minimal toxicity of lead in plants. In
Effect of Heavy Metal Pollution on Plants. Vol. 1. Effects of Trace Metals on Plant
Function (N.W. Lepp, Ed.). Applied Science Publishers, London, New Jersey. pp. 55-
76.
Koeppe, D.E. and Millar, R.J. 1970. Lead effects on corn mitochondrial respiration.
Science 167: 1376-1378.
Körner, C. and Larcher, W. 1988. Plant life in cold environments. In Plants and
36
Temperature, Symp. Soc. Exp. Biol. Vol. 42 (S.F. Long, and F.I. Woodward, Eds.). The
Company of Biologists Limited, Cambridge, pp. 25-57.
Konings, H. and De Wolf, A. 1984. Promotion and inhibition by plant growth regulators
of aerenchyma formation in seedling roots of Zea mays. Physiol. Plant. 60: 309-314.
Krapp, A. and Stitt, M. 1994. Influence of high carbohydrate content on the activity of
plastidic and cytosolic isozyme pairs in photosynthetic tissues. Plant Cell Environ. 17:
861-866.
Kuiper, D. 1983. Genetic differentiation in Plantago major: Growth and root respiration
and their role in phenotypic adaptation. Physiol. Plant. 57: 222-230.
Kuiper, D. and Smid, A. 1985. Genetic differentiation and phenotypic plasticity in
Plantago major ssp. major: I. The effect of differences in level of irradiance on growth,
photosynthesis, respiration and chlorophyll content. Physiol. Plant. 65: 520-528.
Kuiper, D. and Staal, M. 1987. The effect of exogenously supplied plant growth
substances on the physiological plasticity in Plantago major ssp major: Responses of
growth, shoot to root ratio and respiration. Physiol. Plant. 69: 651-658.
Lambers, H. 1979. Efficiency of root respiration in relation to growth rate, morphology
and soil composition. Physiol. Plant. 46: 194-202.
Lambers, H. 1980. The physiological significance of cyanide-resistant respiration in
higher plants. Plant Cell Environ. 3: 293-302.
Lambers, H. 1985. Respiration in intact plants and tissues: Its regulation and dependence
on environmental factors, metabolism and invaded organisms. In Encyclopedia of Plant
Physiology, New Series (R. Douce and D.A. Day, Eds.). Springer-Verlag, Berlin. pp.
418-473.
Lambers, H. 1995. Oxidation of mitochondrial NADH and the synthesis of ATP. In
(Title not yet certain) (D.T. Dennis, D.H. Turpin, D.D. Lefebvre, and D.B. Layzell,
Eds.). Longman Scientific and Technical, in press
Lambers, H. and Atkin. O.K. 1995. Regulation of carbon metabolism in roots. In:
Carbon Partitioning and Source-Sink Interactions in Plants. (M.A. Madore and W.J.
Lucas Eds). American Society of Plant Physiologists, Rockville, pp. 226- 238.
Lambers, H. and Posthumus, F. 1980. The effects of light intensity and relative humidity
on growth rate and root respiration of Plantago lanceolata and Zea mays. J. Exp. Bot.
31: 1621-1630.
Lambers, H. and Van der Werf, A. 1988. Variation in the rate of root respiration of two
Carex species: A comparison of four related methods to determine the energy
requirements for growth, maintenance and ion uptake. Plant Soil 111: 207-211.
37
Lambers, H., Layzell. D.B., and Pate, J.S. 1980. Efficiency and regulation of root
respiration in a legume: Effects of the N-source. Physiol. Plant. 50: 319-325.
Lambers, H., Blacquière, T., and Stuiver, C.E.E. 1981. Interactions between
osmoregulation and the alternative respiratory pathway in Plantago coronopus as
affected by salinity. Physiol. Plant. 51: 63-68.
Lambers, H., Simpson, R.J., Beilharz, V.C., and Dalling, M.J. 1982. Translocation and
utilization of carbon in wheat (Triticum aestivum). Physiol. Plant. 56: 18-22.
Lambers, H., Day, D.A., and Azcón-Bieto, J. 1983. Cyanide-resistant respiration in roots
and leaves. Measurements with intact tissues and isolated mitochondria. Physiol. Plant.
58: 148-154.
Lambers, H., Scheurwater, I., Mata, C. & Nagel, O.W. 1998a. Root respiration of fast-
and slow-growing plants, as dependent on genotype and nitrogen supply: a major clue
to the functioning of slow-growing plants In: Inherent Variation in Plant Growth.
Physiological Mechanisms and Ecological Consequences. H. Lambers, H. Poorter &
M.M.I. Van Vuuren (eds). Backhuys, Leiden, pp. 139-157.
Lambers, H., Chapin, F.S. III, and Pons, T.L. 1998b. Plant Physiological Ecology.
Springer-Verlag, New York.
Lappartient, A.G., Vidmar, J.J., Leustek, T., Glass A.D.M., and Touraine, B. 1999.
Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter
genes expression in roots mediated by phloem-translocated compound. Plant J. 18: 89-
96.
Lennon, A. M., Neuenschwander, U. H., Ribas-Carbo, M., Giles, L., Ryals, J. A. and
Siedow, J. N. (1997). The effects of salicylic acid and tobacco mosaic virus infection on
the alternative oxidase of tobacco. Plant Physiol. 115: 783-791.
Löhr, E. and Müller, D. 1952. Die Respiration von gesunden und viruskranken
Zuckerrüben. Physiol. Plant. 5: 218-220.
Lundegardh, H. 1946. Transport of water and salts through plant tissues. Nature 157:
575-577.
Lundegardh, H. 1955. Mechanisms of absorption, transport, accumulation, and secretion
of ions. Annu. Rev. Plant Physiol. 6: 1-24.
Machlis, L. 1944. The respiratory gradient in barley roots. Am. J. Bot. 31: 281-282.
Markhart, A.H. III. 1982. Penetration of soybean root systems by abscisic acid isomers.
Plant Physiol. 69: 1350-1352.
Massimino, D., André, M., Richaud, C., Massimino, J., and Vivoli, J. 1980. Évolution
horaire au cours d’une journée normale de la photosynthèse, de la transpiration, de la
38
respiration folaire et racinaire et de la nutrition N.P.K. chez Zea mays. Physiol. Plant.
48: 512-518.
Mata, C., Scheurwater, I., Martins-Louçao, M.-A., and Lambers, H. 1996. Root
respiration, growth and nitrogen uptake of Quercus suber L. seedlings. Plant Physiol.
Biochem. 34: 727-734.
Mata, C., Van Vemde, N., Clarkson, D.T., Martins-Loucao, M.A., and Lambers, H.
2000. Influx, efflux and net uptake of nitrate in Quercus suber seedlings. Plant Soil
221: 25-32.
Maxwell, D. P., Wang, Y., and McIntosh, L. (1999). The alternative oxidase lowers
mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci.
USA 96: 8271-8276.
McDonnel, E. and Farrar, J.F. 1992. Substrate supply and its effect on mitochondrial
and whole tissue respiration in barley roots. In Plant Respiration. Molecular,
Biochemical and Physiological Aspects (H. Lambers, and L.H.W. Van der Plas, Eds.).
SPB Academic Publishing, The Hague, pp. 455-462.
Millar, A.H., Wiskich, J.T., Whelan, J., and Day, D.A. 1993. Organic acid activation of
the alternative oxidase of plant mitochondria. FEBS Lett. 329: 259-262.
Millar, A.H., Atkin, O.K., Lambers, H., Wiskich, J.T., and Day, D.A. 1995. A critique
of the use of inhibitors to estimate partitioning of electrons between mitochondrial
respiratory pathways in plants. Physiol. Plant. 95: 523-532.
Millar, A.H., Atkin, O.K., Menz, R.I., Henry, B., Farquhar, G., and Day, D.A. 1998.
Analysis of respiratory chain regulation in roots of soybean seedlings. Plant Physiol.
117: 1083-1093.
Millenaar, F. F., Benschop, J. J., Wagner, A. M. and Lambers, H. 1998. The role of
the alternative oxidase in stabilizing the in vivo reduction state of the ubiquinone pool;
and the activation state of the alternative oxidase. Plant Physiol. 118: 599-607.
Millenaar, F.F., Roelofs, R., Gonzàlez-Meler, M.A., Siedow, J.N. Wagner, A.M., and
Lambers, H. 2000a. The alternative oxidase during low-light conditions. Plant J., 23:
623-632.
Millenaar, F.F., Fiorani, F., Gonzàlez -Meler, M., Welschen, R., Ribas-Carbo, M.,
Siedow, J.N., Wagner, A.M. & Lambers, H. 2000b. Regulation of alternative oxidase
activity in six wild monocotyledonous species; an in vivo study at the whole root
level. Plant Physiol., submitted
Miller, C.O. 1980. Cytokinin inhibition of respiration in mitochondria from six plant
species, Proc. Natl. Acad. Sci. USA 77: 4731-4735.
39
Miller, C.O. 1982. Cytokinin modification of mitochondrial function. Plant Physiol. 69:
1274-1277.
Møller, I.M., and Palmer, J.M. 1982. Direct evidence for the presence of a rotenone-
resistant NADH dehydrogenase on the inner surface of the inner membrane of plant
mitochondria. Physiol. Plant. 54: 267-274.
Neales, T.F. and Davies, J.A. 1966. The effect of photoperiod duration upon the
respiratory activity of the roots of wheat seedlings. Aust. J. Biol. Sci. 19: 471-480.
Nicolas, M.E., Lambers, H., Simpson, R.J., and Dalling, M.J. 1985. Effect of drought on
metabolism and partitioning of carbon in two varieties of wheat differing in drought
tolerance. Ann. Bot. 55: 727-742.
Nobel, P.S. and Palta, J.A. 1989. Soil O2 and CO2 effects on root respiration of cacti.
Plant Soil 120: 263-271.
Osman, A.M. 1971. Root respiration of wheat plants as influenced by age, temperature,
and irradiation of shoots. Photosynthetica 5: 107-112.
Palet, A., Ribas-Carbo, M., Argiles, J.M., and Azcón-Bieto, J. 1991. Short-term effects
of carbon dioxide on carnation callus cell respiration. Plant Physiol. 96: 467-472.
Palet, A., Ribas-Carbo, M., Gonzàlez-Meler, M.A., Aranda, X., and Azcón-Bieto, J.
(1992) Short-term effects of CO2/bicarbonate on plant respiration. In: Molecular,
biochemical and physiological aspects of plant respiration, H. Lambers & L.H.W. Van
der Plas (eds). SPB Academic Publishing, The Hague, pp. 597-602.
Palmer, J.M. 1966. The influence of growth regulating substances on the development
of enhanced metabolic rates in thin slices of beetroot storage tissue. Plant Physiol. 41:
1173-1178.
Palta, J.A. and Nobel, P.S. 1989. Influence of soil O2 and CO2 on root respiration for
Agave deserti. Physiol. Plant. 76: 187-192.
Pang, P.C. and Paul, E.A. 1980. Effects of vesicular-arbuscular mycorrhiza on 14C and
15N distribution in nodulated fababeans. Can. J. Soil. Sci. 60: 241-250.
Pate, J.S., Layzell, D.B., and Atkins, C.A. 1979. Economy of carbon and nitrogen in a
nodulated and nonnodulated (NO3-grown) legume. Plant Physiol. 64: 1083-1088.
Peng, S., Eissenstat, D.M., Graham, J.H., Williams, K., and Hodge, N.C. 1993. Growth
depression in mycorrhizal citrus at high-phosphorus supply. Plant Physiol. 101: 1063-
1071.
Penning de Vries, F.W.T., Brunsting, A.H.M., and Van Laar, H.H. 1974. Products,
40
requirements and efficiency of biosynthetic processes: a quantitative approach. J. Theor.
Biol. 45: 339-377.
Perata, P. and Alpi, A. 1993. Plant responses to anaerobiosis. Plant Sci. 93: 1-17.
Poorter, H. 1991. Interspecific variation in the relative growth rate of plants: the
underlying mechanisms. PhD Thesis, Utrecht University.
Poorter, H., Remkes, C., and Lambers, H. 1990. Carbon and nitrogen economy of 24
wild species differing in relative growth rate. Plant Physiol. 94: 621-627.
Poorter, H., van der Werf, A., Atkin, O.K., and Lambers, H. 1991. Respiratory energy
requirements of roots vary with the potential growth rate of a plant species. Physiol.
Plant. 83: 469-475.
Purvis, A. C. and Shewfelt, R. L. 1993. Does the alternative pathway ameliorate
chilling injury in sensitive plant tissues? Physiol. Plant. 88: 712-718.
Qi, J., Marshall, J.D., and Mattson, K.G. 1994. High soil carbon dioxide concentrations
inhibit root respiration of Douglas fir. New Phytol. 128: 435-442.
Reid, M.S. and Prat, H.K. 1972. Effects of ethylene on potato tuber respiration. Plant
Physiol. 49: 252-255.
Ribas-Carbo, M., Berry, J.A., Yakir, D., Giles, L., Robinson, S.A., Lennon, A.M., &
Siedow, J.N. (1995) Electron partitioning between the cytochrome and alternative
pathways in plant mitochondria. Plant Physiol. 109: 829-837.
Roberts, J.K.M., Wemmer, D., and Jardetzky, O. 1984. Measurements of mitochondrial
ATP-ase activity in maize root tips by saturation transfer 31P nuclear magnetic
resonance. Plant Physiol. 74: 632-639.
Rychter, A.M. and Mikulska, M. 1990. The relationship between phosphate status and
cyanide-resistant respiration in bean roots. Physiol. Plant. 79: 663-667.
Rychter, A., Janes, H.W., and Frenkel, C. 1978. Effect of ethylene and oxygen on the
development of cyanide-resistant respiration in whole potato mitochondria. Plant
Physiol. 63: 149-151.
Rychter, A.M., Chauveau, M., Bomsel, J.-L., and Lance, C. 1992. The effect of
phosphate deficiency on mitochondrial activity and adenylate levels in bean roots.
Physiol. Plant. 84: 80-86.
Ryle, G.J.A., Arnott, R.A., Powell, C.E., and Gordon, A.J. 1984. N2 fixation and the
respiratory costs of nodules, nitrogenase activity, and nodule growth and maintenance in
Fiskeby soyabean. J. Exp. Bot. 35: 1156-11651.
41
Ryle, G.J.A., Powell, C.E., and Gordon, A.J. 1985a. Short term changes in CO2.
evolution associated with nitrogenase activity in white clover in response to defoliation
and photosynthesis, J. Exp. Bot. 36: 634-643.
Ryle, G.J.A., Powell, C.E., and Gordon, A.J. 1985b. Defoliation in white clover:
Regrowth, photosynthesis and N2 fixation. Ann. Bot. 56: 9-18.
Saglio, P.H. and Pradet, A. 1980. Soluble sugars, respiration, and energy charge during
aging of excised maize root tips. Plant Physiol. 66: 516-519.
Scheurwater, I. (1999) Why do fast- and slow-growing grass species differ less than
expected in their rate of root respiration? PhD Thesis, Utrecht University, Utrecht, the
Netherlands.
Scheurwater, I., Cornelissen, C., Dictus, F. Welschen, R., and Lambers, H. 1998. Why
do fast- and slow-growing grass species differ so little in their rate of root respiration,
considering the large differences in rate of growth and ion uptake? Plant Cell Environ.
21: 995-1005.
Scheurwater, I., Clarkson, D.T., Purves, J., Van Rijt, G., Saker, L., Welschen, R., and
Lambers, H. 1999. Relatively large nitrate efflux can account for the high specific
respiratory costs for nitrate transport in slow-growing grass species. Plant Soil 215:
123-134.
Scheurwater, I., Dünnebacke, M., Eising, R., and Lambers, H. 2000. Respiratory costs
and rate of protein turnover in the roots of a fast- and a slow-growing grass species. J.
Exp. Bot. 51: 1089-1097.
Schubert, S., Schubert, E., and Mengel, K. 1990. Effect of low pH of the root medium
on proton release, growth, and nutrient uptake of field beans (Vicia faba). Plant Soil
124: 239-244.
Silsbury, J.H., Smith, S.E., and Oliver, A.J. 1983. A comparison of growth efficiency
and specific rate of dark respiration of uninfected and vesicular-arbuscular mycorrhizal
plants of Trifolium subterraneum L. New Phytol. 93: 555-566.
Singh, J.N. and Singh, J.N. 1971. Studies on the physiology of host-parasite
relationships in Orobanche. I. Respiratory metabolism of host and parasite. Physiol.
Plant. 24: 380-386.
Smakman, H. and Hofstra, R. 1982. Energy metabolism of Plantago lanceolata as
affected by change in root temperature. Physiol. Plant. 56: 33-37.
Snellgrove, R.C., Splittstoesser, W.E., Stribley, D.P., and Tinker, P.B. 1982. The
distribution of carbon and the demand of the fungal symbiont in leek plants with
vesicular-arbuscular mycorrhizas. New Phytol. 92: 75-87.
42
Solomos, T. and Laties, G.G. 1976. Induction by ethylene of cyanide-resistant
respiration. Biochem. Biophys. Res. Comm. 70: 663-671.
Sowell, J.B. and Spomer, G.G. 1986. Ecotypic variation in root respiration rate among
elevational populations of Abies lasiocarpa and Picea engelmannii. Oecologia 68: 375-
379.
Steingröver, E. 1981. The relationship between cyanide-resistant root respiration and the
storage of sugars in the taproot in Daucus carota L. J. Exp. Bot. 32: 911-919.
Stolwijk, J.A.J. and Thimann, K.V. 1957. On the uptake of carbon dioxide and
bicarbonate by roots and its influence on growth. Plant Physiol. 32: 513-520.
Szaniawski, R.K. 1981. Shoot:root functional equilibria. Thermodynamic stability of the
plant system. In Structure and Function of Plant Roots (R. Brouwer, O. Gasparikova, J.
Kolek, and B.G. Loughman, Eds.) Martinus Nijhoff/Dr W. Junk Publishers, The Hague,
pp. 357-360.
Szaniawski, R.K. and Kielkiewicz, M. 1982. Maintenance and growth respiration in
shoots and roots of sunflower plants grown at different root temperatures. Physiol. Plant.
54: 500-504.
Taleisnik, E.L. 1987. Salinity effects on growth and carbon balance in Lycopersicon
esculentum and L. pennellii. Physiol. Plant. 71: 213-218.
Tan, K. and Keltjens, W.G. 1990a. Interaction between aluminium and phosphorus in
sorghum plants. I. Studies with the aluminium sensitive genotype TAM428. Plant Soil
124: 25-23.
Tan, K. and Keltjens, W.G. 1990b. Interaction between aluminium and phosphorus in
sorghum plants. II. Studies with the aluminium tolerant genotype SC0 283. Plant Soil
124: 25-32.
Theologis, A. and Laties, G.G. 1978. Relative contribution of cytochrome-mediated and
cyanide-resistant electron transport in fresh and aged potato slices. Plant Physiol. 62:
232-237.
Tjepkema, J.D. and Winship, L.J. 1980. Energy requirement for nitrogen fixation in
actinorhyzal and legume root nodules. Science 209: 279-281.
Tredici, M.R., Margheri, M.C., Giovannetti, L., De Philippis, R., and Vincenzini, M.
1988. heterotrophic metabolism and diazotrophic growth of Nostoc sp. from Cycas
circinalis. Plant Soil 110: 199-207.
Trought, M.C.T., and Drew, M.C. 1980. The development of waterlogging damage in
young wheat plants in anaerobic solution cultures. J. Exp. Bot. 31: 1573-1585.
43
Umbach, A.L. and Siedow, J.N. 1993. Covalent and noncovalent dimers of the cyanide-
resistant alternative oxidase protein in higher plant mitochondria and their relationship
to enzyme activity. Plant Physiol. 103: 845-854.
Umbach, A.L., Wiskich, J.T., and Siedow, J.N. 1994. Regulation of alternative oxidase
kinetics by pyruvate and intermolecular disulfide bond redox status in soybean
mitochondria. FEBS Lett. 348: 181-184.
Uritani, I. and Asahi, T. 1980. Respiration and related metabolic activity in wounded
and infected tissues. In The Biochemistry of Plants. Vol. 2 Metabolism and Respiration
(D.D. Davies, Ed.). Academic Press, London, pp. 463-485.
Van Beusichem, M.L. 1982. Nutrient absorption by pea plants during dinitrogen
fixation. 2. Effects of ambient acidity and temperature. Neth. J. Agric. Sci. 30: 85-97.
Van den Bergen, C.W.M., Wagner, A.M., Krab, K., and Moore, A.L. 1994. The
relationship between electron flux and the redox poise of the quinone pool in plant
mitochondria; Interplay between quinol-oxidizing and quinone-reducing pathways.
FEBS Lett. 226: 1071-1078.
Van der Werf, A., Kooijman, A., Welschen, R., and Lambers, H. 1988. Respiratory
costs for the maintenance of biomass, for growth and for ion uptake in roots of Carex
diandra and Carex acutiformis. Physiol. Plant. 72: 483-491.
Van der Werf, A., Raaimakers, D., Poot, P., and Lambers, H. 1991. Evidence for a
significant contribution of peroxidase-mediated O2-uptake to root respiration of
Brachypodium pinnatum. Planta 183: 347-352.
Van der Werf, A., Welschen, R., and Lambers, H. 1992a. Respiratory losses increase
with decreasing inherent growth rate of a species and with decreasing nitrate supply: a
search for explanations for these observations. In Molecular, Biochemical and
Physiological Aspects of Plant Respiration (H. Lambers, and L.H.W. Van der Plas,
Eds.). SPB Academic Publishing, The Hague, pp. 421-432.
Van der Werf, A., Van den Berg, G., Ravenstein, H.J.L., Lambers, H., and Eising, R.
1992b. Protein turnover: A significant component of maintenance respiration in roots?
In Molecular, Biochemical and Physiological Aspects of Plant Respiration (H. Lambers,
and L.H.W. Van der Plas, Eds.). SPB Academic Publishing, The Hague, pp. 483-492.
Van der Werf, A.K., Schieving, F., and Lambers, H. 1993. Evidence for optimal
partitioning of biomass and nitrogen at a range of nitrogen availabilities for a fast- and
slow-growing species. Func. Ecol. 7: 63-74.
Van der Werf, A., Poorter, H., and Lambers, H. 1994. Respiration as dependent on a
species’s inherent growth rate and on the nitrogen supply to the plant. In A Whole-Plant
Perspective of Carbon-Nitrogen Interactions (J. Roy, and E. Garnier, Eds.). SPB
44
Academic Publishing, pp. 61-77.
Vanlerberghe, G.C., Vanlerberghe, A.E., and McIntosh, L. 1994. Molecular genetic
alteration of plant respiration. Silencing and overexpression of alternative oxidase in
transgenic tobacco. Plant Physiol. 106: 1503-1510.
Veen, B.W. 1977. The uptake of potassium, nitrate, water, and oxygen by a maize root
system in relation to its size. J. Exp. Bot. 28: 1389-1398.
Veen, B.W. 1980. Energy costs of ion transport. In Genetic Engineering of
Osmoregulation. Impact on Plant Productivity for Food, Chemicals and Energy (D.W.
Rains, R.C. Valentine, and A. Hollaender, Eds.), Plenum, New York, pp. 187-195.
Wagner, A. M. and Krab, K. (1995). The alternative respiration pathway in plants:
Role and regulation. Physiol. Plant. 95: 318-325.
Wang, S.Y., Steffens, G.L., and Faust, M. 1983. Occurrence of alternative respiratory
pathway in freshly excised apple root tissue. J. Amer. Soc. Hort. Sci. 108: 1059-1064.
Wanner, H. 1950. Histologische und physiologische Gradienten in der Wurzelspitze.
Ber. Schweiz. Bot. Gesellsch. 60: 404-412.
Wanner, H., and Schmucki, S. 1950. Hemmung der Wurzelatmung durch
Ausscheidungen des Wurzelsystems. Ber. Schweiz. Bot. Gesellsch. 60: 413-425.
Weger, H.G. and Guy, R.D. 1991. Cytochrome and alternative pathway respiration in
white spruce (Picea glauca) roots. Effects of growth and measurement temperature.
Physiol. Plant 83: 675-681.
Whipps, J.M. 1987. Carbon loss from the roots of tomato and pea seedlings grown in
soil. Plant Soil 103: 95-100.
Williams, J.H.H. and Farrar, J.F. 1990. Control of barley root respiration. Physiol. Plant.
79: 259-266.
Williams, J.H.H. and Farrar, J.F. 1992. Substrate supply and respiratory control. In Plant
Respiration. Molecular, Biochemical and Physiological Aspects (H. Lambers, and
L.H.W. Van der Plas, Eds.). SPB Academic Publishing, The Hague, pp. 471-475.
Williams, J.H.H., Minchin, P.E.H., and Farrar, J.F. 1991. Carbon partitioning in split
root systems of barley: the effect of osmotica. New Phytol. 42: 453-460.
Williams, J.H.H., Winters, A.L., and Farrar, J.F. 1992. Sucrose: a novel plant growth
regulator. In Plant Respiration. Molecular, Biochemical and Physiological Aspects (H.
Lambers, and L.H.W. Van der Plas, Eds.). SPB Academic Publishing, The Hague, pp.
463-469.
45
Williamson, R.E. 1968. Influence of gas mixtures on cell division and root elongation of
broad bean, Vicia faba L.. Agronomy J. 60: 317-321.
Williamson, R.E. and Splinter, W.E. 1968. Effects of gaseous composition of root
environment upon root development and growth of Nicotiana tabacum L.. Agronomy J.
60: 365-368.
Willis, A.J. and Yemm, E.W. 1955. Respiration of barley plants. VIII. Nitrogen
assimilation and the respiration of the root system. New Phytol. 54: 163-181.
Winship, L.J. and Tjepkema, J.D. 1982. Simultaneous measurement of acetylene
reduction and respiratory gas exchange of attached root nodules. Plant Physiol. 70:
361-365.
Yan, F., Schubert, S., and Mengel, K. 1992. Effect of low root medium pH on net
proton release, root respiration, and root growth of corn (Zea mays L.) and broad bean
(Vicia faba L.). Plant Physiol. 99: 415-421.
Yemm, E.W. 1965. The respiration of plants and their organs. In Plant Physiology, A
Treatise, Vol. VIA (F.C. Steward, Ed.). Academic Press, New York, pp. 231-310.
Zacheo, G. and Molinari, S. 1987. Relationship between root respiration and seedling
age in tomato cultivars infested by Meloidogyne incognita. Ann. Appl. Biol. 111:
589-595.
Zimmermann, R.C, Smith, R.D., Alberte, R.S. 1989. Thermal acclimation and whole-
plant carbon balance in Zostera marina L. (eelgrass). J. Exp. Mar. Biol. Ecol. 130: 93-
109.
46
Figure legends
FIGURE 1 Carbohydrate consumption in root respiration as a proportion of those
produced in photosynthesis for 24 herbaceous species, grown in a nutrient solution with
an optimum supply of nitrate. [Based on data from Poorter et al. (1990).]
FIGURE 2 Rate of O2 consumption by primary roots of Allium cepa and the number of
cells per cubic millimeter of root as a function of the distance from the tip. Data are
expressed per gram of nitrogen (circles) and per cell (squares). [Based on data from
Wanner (1950).]
FIGURE 3 Diurnal course of the soluble sugar concentration (A), and the rate of CO2
production (B) in the roots of Cucumis sativus. The data are expressed on the basis of
starch- and sugar-free dry mass. [Based on data from Challa (1976).]
FIGURE 4 Respiration of excised apical 40-mm root segments of Pisum sativum as
dependent on the concentration and time after addition of exogenous sucrose. The dots
refer to the original measurements, the plane was calculated using a graphics program
(Surf, version 3.00, copyright Golden Software, Inc., 1987). [Based on data from Bryce
and ap Rees (1985a).]
FIGURE 5 Diurnal variation in the rate of O2 consumption (nmol O2 g-1 (DM) s-1, filled
symbols) and CO2 production (nmol CO2 g-1 (DM) s-1, open symbols) by roots of
Holcus lanatus growing in nutrient solution with 2 mM nitrate. The light period started
at 5 a.m. and finished at 7 p.m.. Due to greater variation in CO2 production than in O2
consumption, the respiratory quotient (RQ) varies diurnally. [Based on data from
Scheurwater et al., 1998.]
FIGURE 6 (A) Rate of O2 consumption (µmol (g FM)-1 day-1) in roots of Carex
acutiformis and C. diandra as related to both the relative growth rate (RGR) of the roots
and their net rate of anion uptake (NIR). (B) Rate of O2 consumption (µmol (g FM)-1
day-1) in roots of Quercus suber as related to the relative growth rate of the roots. The
plane in (A) and line in (B) give the predicted mean rate of O2 consumption. The
symbols are experimentally determined points (and SE, n = 6 and 8?? in (A) and (B),
respectively). The intercept of the plane in (A) and the line in (B) with the y-axis gives
m. The slope of the projection of the line on the y-z plane gives 1/YGR; when projected
on the x-y plane, the slope gives 1/UI. In (B) the slope gives costs for growth including
ion uptake. [(A) Based on data from Van der Werf et al. (1988); (B) based on data from
Mata et al. (1998).]
FIGURE 7 Respiratory energy budgets for roots of 24 herbaceous species, grown in a
nutrient solution with nitrate. The budgets were constructed assuming that the specific
costs for maintenance are the same for all species, i.e. similar to the ones for Carex
diandra (Fig. 6). Costs for growth were calculated from the roots’ biochemical
composition and the remaining part of the experimentally determined rate of O2
consumption was then apportioned to ion uptake. [Based on data from Poorter et al.
(1991).]
47
FIGURE 8 Root respiration and sorbitol accumulation in the roots of Plantago
coronopus. (A) SHAM-resistant root respiration, (B) SHAM-sensitive respiration, and
(C) sorbitol accumulation. Plants were pregrown in a nonsaline nutrient solution and
transferred at time zero to a nutrient solution containing 50 mol m-3 NaCl (closed
symbols). Control plants (open symbols) were kept in a nonsaline solution throughout.
[Based on data from Lambers et al. (1981).]
FIGURE 9 The activity (nmol O2 g-1 FM-1) in Poa annua roots of the alternative
oxidase (circles) and cytochrome pathway (squares) with sucrose (open symbols) or
without sort-term sucrose addition (closed symbols). Measurements were made with the
18O isotope-fractionation technique and at different times after the transfer to low-light
conditions. Error bars represent standard error (n=2 to 5). [Based on data from Millenaar
et al. (2000a).]
FIGURE 10 Immunoblot of alternative oxidase in whole-root extracts of Poa annua at
different times after the transfer to low light conditions (0=control, and day 1, 2 and 3
after the transfer). [Based on data from Millenaar et al. (2000a).]
48
TABLE 1 Utilization of carbohydrates for root respiration as a percentage of those translocated to the roots.
Only nonsymbiotically grown plants are included. If necessary, values were recalculated from data presented
in the literature, assuming 40% C in the dry matter and a respiratory quotient of 1.0.
_____________________________________________________________________________________
Species Utilization Special remarks Reference
for root
respiration
_____________________________________________________________________________________
Daucus carota 29-53 Decreases upon Steingröver (1981)
tap root formation
Festuca ovina 54 Atkinson and Farrar (1983)
Glycine max 38 Harris et al. (1985)
Helianthus annuus 67 Hatrick and Bowling (1973)
H. annuus 35-44 Szaniawski and Kielkiewicz (1982)
Hordeum distichum 41 Farrar (1985)
H. vulgare 15 High N Johansson (1992)
19 Low N
Monocotyledons with 32 High nutrient supply Van der Werf et al. (1992a)
a high potential growth rate
Monocotyledons with 60 Low N Van der Werf et al. (1992a)
a high potential growth rate supply
Monocotyledons with 51 High nutrient Van der Werf et al. (1992a)
a low potential growth rate supply
Monocotyledons with 54 Low N Van der Werf et al. (1992a)
a low potential growth rate supply
Nardus stricta 50 Atkinson and Farrar (1983)
Pisum sativum 52-60 NO3--fed De Visser (1985)
Triticum aestivum 67 Seedlings, Barneix et al. (1984)
Pre-grown in CaSO4
T. aestivum 52 Sand-grown, Lambers et al. (1982)
nutrient-limited
Zea mays 44-57 Excised root tips, Kandler (1953)
cultivated in vitro
Z. mays 49 Veen (1980)
_____________________________________________________________________________________
49
TABLE 2 Utilization of carbohydrates for daily root respiration as a percentage of those produced daily in
photosynthesis. When the plants were grown in soil, part of the respiration may be due to respiration of
microorganisms.
__________________________________________________________________________
Species Utilization Special remarks Reference
for root
respiration
%
__________________________________________________________________________
Allium porrum 18 Nonmycorrhizal Snellgrove et al. (1982)
23 Mycorrhizal
Cucumis sativus 12 High light+long days Challa (1976)
14 Low light +short days
Daucus carota 14-19 Decreases with age Steingröver (1981)
Deschampsia 24 High light Poorter (1991)
flexuosa 25 Low light
Festuca ovina 31 Atkinson and Farrar (1983)
F. pratensis 15 Grown in soil Johansson (1991)
Galinsoga parviflora 8 High potential growth rate Poorter et al. (1990)
Glycine max 9 Nonsymbiotic Harris et al. (1985)
15 With Rhizobium
28 With Rhizobium+Glomus
Helianthus annuus 13-15 Szaniawski (1981)
Holcus lanatus 17 High light Poorter (1991)
17 Low light
Hordeum distichum 14 Farrar (1981)
Lolium multiflorum 14-20 High at low light Hansen and Jensen (1979)
Lupinus albus 23 Nonnodulated Pate et al. (1979)
35 With Rhizobium
Lycopersicon esculentum 9-18 Increases with age; grown in soil Whipps (1987)
Nardus stricta 21 Atkinson and Farrar (1983)
Pisum sativum 12-18 Nonnodulated; NO3--fed; De Visser (1985)
decreases with age
16-20 With Rhizobium; decreases with age
P. sativum 25 Duarte et al. (1988)
P. sativum 21-24 Nonnodulated; grown in soil Whipps (1987)
decreases with age
Zea mays 18? 56 days old Massimino et al. (1980)
Monocots with a high 18? High nutrient supply Van der Werf et al. (1992a)
potential growth rate 52 Low nutrient supply
Monocots with a low 16 High nutrient supply Van der Werf et al. (1992a)
potential growth rate 38 Low nutrient supply
_______________________________________________________________________
50
TABLE 3. The activity of the alternative path, assessed using the oxygen –isotope discrimination technique. Rates are
expressed as a percentage f the control rate, expressed in nmol O2 (g DM)-1 s-1. All plants were grown in nutrient
solution.
_________________________________________________________________________________________
Species Alternative Control Special Reference
path activity rate remarks
(%) (nmol O2 g-1 FM s-1)
_________________________________________________________________________________________
Glycine max 5 4.1 4-days-old Millar et al., 1998
G. max 34 3.8 7-days-old ,,
G. max 54 1.6 17-days-old ,,
G. max 37 1.7 14oC Gonzàlez-Meler et al., 1999
G. max 43 5.7 28oC ,,
Nicotiana tabacum 30 2.0 Lennon et al., 1997
Poa alpina 22 3.1 Millenaar et al., 2000b
P. annua 30 4.0 ,,
P. annua 48 1.5 low light Millenaar et al., 2000a
P. compressa 11 3.4 Millenaar et al., 2000b
P. pratensis 13 4.5 ,,
P. trivialis 49 4.0 ,,
Vicia radiata 11 1.5 19oC Gonzàlez-Meler et al., 1999
V. radiata 18 1.3 28oC ,,
_________________________________________________________________________________________
51
TABLE 4. The respiratory quotient (RQ) of root respiration of a number of herbaceous and woody species. All plants
were grown in nutrient solution, with nitrate as the N-source, unless stated otherwise. The barley plants used by Willis
and Yemm (1955) were pre-grown without a nitrogen source and then provided with no N, ammonia or nitrate at the
start of the respiration measurements. The pea plants used by De Visser (1985) were grown with a limiting supply of
combined N, so that their growth rate matched that of the symbiotically grown plants.
___________________________________________________________________________
Species RQ Special Reference
Remarks
___________________________________________________________________________
Allium cepa 1.0 Root tips Berry (1949)
1.3 Basal parts
Avicennia marina 1.0 Burchett et al. (1984)
A. marina 0.85 Fine roots Curran et al. (1986)
0.82 Cable roots
Dactylis glomerata 1.2 NO3-fed Scheurwater et al. (1998)
Festuca ovina 0.95 NO3-fed
Galinsoga parviflora 1.64 NO3-fed I. Scheurwater, unpublished
Helianthus annuus 1.53 NO3-fed ,,
Holcus lanatus 1.3 NO3-fed ,,
Hordeum distichum 1.03 NO3-fed Williams and Farrar (1990)
H. vulgare 1.22 NH4-fed Bloom et al. (1992)
1.09 NO3-fed
H. vulgare 0.94 Root tips Machlis (1944)
0.97 Basal parts
H. vulgare 0.90 N-deprived Willis and Yemm (1955)
0.95 NH4+ added
1.70 NO3- added
Lupinus albus 1.4 NO3--fed Lambers et al. (1980)
1.6 N2-fixing
Oryza sativa 1.0 NH4+-fed Brambilla et al. (1986)
1.13 NO3- -fed
Pisum sativum 0.84 NH4--fed De Visser (1985)
0.95 NO3--fed
1.42 N2-fixing
Triticum aestivum 1.15 0-4 mm Karlsson and Eliasson (1955)
1.0 Basal parts
T. aestivum 1.5 N-deprived Barneix et al. (1984)
1.1 NH4+ added
2.0 NO3- added
Zea mays 1.0 Basal parts Greenway and West (1973)
Z. mays 1.0 Fresh tips Saglio and Pradet (1980)
0.75 Starved tips
___________________________________________________________________________
52
TABLE 5. The in vivo ADP:O ratios in root tips of Zea mays, as determined with the saturation transfer 31P-NMR
technique and O2 uptake measurements. Rates of ATP production and O2 consumption are expressed as nmol g-1
(FM) s-1. Exogenous glucose and succinate were supplied at 50 mol m-3. The concentration of KCN was 0.5 mol m-
3 and that of SHAM 2 mol m-3, which is sufficiently high to fully block the alternative path in maize root tips (H.
Lambers unpublished). Only mean values are presented, so that the ADP:O ratio cannot be calculated from the
primary data given in the table. (Data from Roberts et al., 1984.)
___________________________________________________________
Exogenous O2 Inhibitor Rate of Rate of ADP:O
substrate concen- O2 ATP ratio
tration uptake production
___________________________________________________________
Glucose 100 None 22.3 142.6 3.19
Glucose 0 None 0 <20 -
None 100 None 14.9 93.0 3.03
Glucose 100 KCN 13.7 26.2 0.96
Glucose 100 KCN+SHAM 3.7 <20 -
Glucose 100 SHAM 21.1 136.7 3.24
Succinate 100 None 16.1 63 1.96
___________________________________________________________
53
TABLE 6. Control of Respiration of Intact Roots by Adenylates, via Their Effect on the Cytochrome path
(A, Zea mays), or via Their Effect on the Substrate Supply to the Mitochondria (B, Phaseolus vulgaris).
[Data from Day and Lambers (1983).]
___________________________________________
Conditionsa Oxygen consumptionb (%)
___________________________________________
A. None 100
+ KCN 47
+ SHAM 70
+ CCCP 141
+ SHAM + CCCP 91
B. None 100
+ KCN 69
+ SHAM 95
+ CCCP 122
+ SHAM + CCCP 92
___________________________________________
aApplied concentrations: CCCP, 2 mmol m-3; SHAM, 10 mol m-3; KCN, 0.5 mol m-3.
bRates are expressed as percentages of the basal rate [64 and 89 nmol (g DM)-1 s-1 for Z. mays and P.
vulgaris, respectively].
54
TABLE 7. (A) Specific respiratory energy costs for the maintenance of root biomass, for root growth
and for ion uptake. The values were obtained using a multiple regression analysis, as explained in
Figure 25A (Van der Werf et al. 1988: average values for Carex acutiformis and C. diandra (sedges);
Bouma et al. 1996: Solanum tuberosum; Veen 1980: Zea mays). (B) Specific respiratory energy costs
for the maintenance of root biomass and for root growth including costs for ion uptake. The values
were obtained using a linear regression analysis, as explained in Figure 25B (Scheurwater et al. 1998:
Dactylis glomerata and Festuca ovina; Mata et al. 1996: Quercus suber; R. Van den Boogaard,
unpublished: Triticum aestivum).
A.
_____________________________________________
Carex Solanum Zea
_____________________________________________
Growth, 6.3 10.9 9.9
mmol O2 (g DM)-1
Maintenance, 5.7 4.0 12.5
nmol O2 (g DM)-1 s-1
Anion uptake, 1.0 1.2 0.53
mol O2 (mol ions)-1
_____________________________________________
B.
_______________________________________________________________
Dactylis Festuca Quercus Triticum
_______________________________________________________________
Growth + ion uptake, 11 19 12 18
mmol O2 (g DM)-1
Maintenance, 26 21 6 22
nmol (g DM)-1 s-1
_______________________________________________________________
55
Time (hours)
010 20 30 40 50 60 70 80 90 100
Oxygen uptake (nmol O
2
g
-1
FM s
-1
)
0
1
2
3
4
valt
vcyt
valt + sucrose
vcyt + sucrose
56
FIGURE 11.
57