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Carbohydrate Reserves, Translocation, and Storage in
Woody Plant Roots
Wayne H. Loescher, Thaddeus McCamant, and John D. Keller
Department of Horticulture and Landscape Architecture, Washington State University,
Pullman, WA 99164-6414
All of the perennial organs of a woody plant may serve a storage
function, but the highest concentrations of carbohydrate reserves
are usually found in root tissues. These root reserves change dra-
matically throughout the year, decreasing rapidly with budbreak and
early vegetative and reproductive development, and then increasing
late in the growing season, usually after cessation of vegetative
growth and fruit maturation. Accumulation of these reserves is very
sensitive to late-season stresses and management practices, and de-
creased accumulation can profoundly affect a tree’s performance
the following year. These root reserves apparently play important
and specific roles in supplying substrates for shoot respiration and
growth, especially in woody species that flower and begin fruit
development before substantial canopy development. Although
phloem transport may be involved in root-to-shoot transport, con-
siderable xylem transport occurs in some early flowering and fruit-
ing species. Regulation of mobilization of root reserves remains
unclear, but both gibberellins and auxins are possibly involved.
Unfortunately, despite their apparent importance, mobilization,
transport and the specific functions of root reserve carbohydrates
are only superficially defined for any woody plant.
nearly fully expanded before anthesis, and much of fruit develop-
ment occurs late in the season, long after canopy development.
Hansen (1971) reported that apple flowers depend on reserves only
during their earliest stages of development, or until the first five or
six leaves have formed. Once petals emerge from the sepals, pho-
tosynthesis from the leaves becomes the major source of carbohy-
drates for flower and fruit growth. Most of the apple reserves are
apparently used in respiration rather than for new building materials
(Hansen and Grausland, 1973), and, in young apple rootstocks,
< 20% of [
14
C]-labeled reserves assimilated in fall was fixed in new
growth the following season (Hansen, 1967; Kandiah, 1979b). Tromp
(1983) concluded that, while apple roots do certainly supply above-
ground parts with carbohydrates early in the spring, it was doubtful
whether such contributions are significant, and it was likely that
reserves are used mostly in respiration.
IMPORTANCE OF CARBOHYDRATE RESERVES
We are certain that reserves, especially stored carbohydrates, play
essential roles in all trees. We know that, by the end of a growing
season, tree roots will generally contain higher concentrations of
carbohydrates and other reserves than any other tissues or organs.
Nevertheless, we know very little about what specific roles these
compounds play in tree survival, growth, and development. In ad-
dition, it is not clear what these materials are (Glerum, 1980), where
they are stored, how they are mobilized or transported, or if they
play any particular roles outside the roots. For most woody species,
the specific roles of root carbohydrates and other root reserves in
respiration during dormancy, in shoot expansion, in stem and root
diameter growth, in new root length growth, in fruit set, and in
flower bud initiation and development are almost completely un-
known.
It is, however, clear that reserves must be used in new leaf growth
in all deciduous species. When nonbearing apple (Quinlan, 1969)
and pecan (Lockwood and Sparks, 1978a) were fed
14
CO
2
in the
fall, radioactivity appeared in all new leaf and shoot growth the
following spring. The same experiment on bearing pecan trees also
showed that staminate and pistillate flowers used reserves (Lock-
wood and Sparks, 1978b). When bearing pecan shoots were fed
14
CO
2
, photosynthates were not exported until after pistillate an-
thesis,
≈3
weeks after budbreak (Davis and Sparks, 1974), indi-
cating that both root and secondary growth were entirely dependent
on reserves until that time.
Reserves throughout woody plants are certainly important for
several reasons. Winter survival depends on adequate reserves. The
importance of respiration is clear. Buds often undergo some growth
and development throughout the dormant season. In the seasonally
dry tropics, many woody plants are deciduous, or nearly so, during
the dry season (Opler et al., 1976). Yet, respiration continues, and
reproductive development may occur in some species, e.g., Antiaris
africana Engl. (Olofinboba, 1969), resulting in considerable reduc-
tion in and total reliance on reserves. In some temperate deciduous
woody species, flowering also occurs before vegetative develop-
ment, and the early stages of reproductive growth must be totally
dependent on reserves. Most willows, poplars, birches, and maples
are specific examples of temperate species in which anthesis and
even substantial fruit development occur before leaf expansion and
photosynthetic competence (Fowells, 1965).
Although grapes are like apples and do not flower and begin
cluster development until after several leaves have expanded,
14
CO
2
labeling experiments showed that sugars manufactured in leaves in
the fall (after harvest) and converted to starch in the wood and roots
are the first carbohydrates used by new shoots the following spring
(Kliewer and Leach, unpublished data, cited by Winkler et al., 1974).
New grape shoots depend on these reserves until the first few leaves
on the shoot are about half their full size, at which time they start
exporting more photosynthate than they import (Hale and Weaver,
1962; Koblet, 1969, cited by Winkler et al., 1974). Therefore, it is
clearly important that grape leaves remain active after harvest to
establish carbohydrate reserves in root storage tissue for leaf growth
and fruit cluster development the following spring.
What are the carbohydrate reserves in roots?
A tree may be 70% to 75% carbohydrates, but determining which
of these play storage roles and contribute to early growth of res-
piration during dormancy presents some formidable analytical dif-
ficulties. Carbohydrate reserves generally include both soluble and
insoluble substances, requiring several specific techniques for ex-
traction and qualitative and quantitative assay. Roots present ob-
vious sampling problems. Also, although the discussion here
emphasizes carbohydrates, other compounds, especially nitrogen-
ous reserves (Titus and Kang, 1982), play important and essential
roles.
Among deciduous fruits and nuts (the focus of this discussion),
the importance of reserves to reproductive growth depends in part There is no evidence suggesting that roots contain unique car-
on the timing of flower and fruit development. Similar to willows
bohydrate reserves. There are, however, qualitative differences. For
and birches, stone fruits and pecans must rely on reserves for a
example, of the soluble carbohydrates, sucrose is the major pho-
while, since these species generally flower before canopy devel- tosynthetic product in many plants, the principal transportable car-
opment (Westwood, 1978), although fruit development may occur
bohydrate, and the main storage sugar (ap Rees, 1984), but its
after full leaf expansion. Other deciduous fruits may be less depen- presence is limited in woody roots. The hexose-reducing sugars,
dent on reserves. Apple leaves on fruiting spurs are, for example, fructose and glucose, are commonly present in roots at higher con-
centrations than sucrose, whereas they are usually at lower concen-
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trations in above-ground parts. And, while both reducing and most
nonreducing sugars like sucrose have routinely been detected and
quantified in roots in the past, the methods used often did not detect
sugar alcohols. Sugar alcohols, as nonreducing carbohydrates, are
common constituents of many plants. Sorbitol in the Rosaceae, or
more commonly mannitol in other families (e.g., the Oleaceae,
Rubiaceae, Scrophulariaceae, and Apiaceae) may be the principal
photosynthetic product, the major transport substance, and an im-
portant storage compound in leaves and other tissues (Lewis, 1984;
Loescher, 1987), but sugar alcohols appear to be only minor com-
ponents of roots. Failure to account for sugar alcohols, however,
in plants now known to be major producers of these compounds,
is a major defect in some older research and occasionally in more
recent literature.
Many other soluble carbohydrates, such as inositol, xylose,
rhamnose, maltose, trehalose, arabinose, ribose, mannose, and gal-
actose, as well as the sucrose derivatives raffinose and stachyose,
are now known to occur in low amounts in both roots and shoots.
Among these, raffinose has been identified as a storage carbohy-
drate, particularly during dormancy in several tree fruits shoots and
roots (Keller and Loescher, 1989; Lasheen and Chaplin, 1977).
Fructans, fructose polymers of various sizes, are common in grasses
and several other important taxa (Pollock, 1986), but evidence of
their presence in deciduous fruit trees is lacking for either shoots
or roots.
Starch is ubiquitous and usually the main insoluble storage car-
bohydrate in most above-ground woody plant tissues, but, in sweet
cherry leaves, soluble carbohydrates, mainly sorbitol, accumulate
more than starch (Roper et al., 1988). Wood ray parenchyma, how-
ever, in shoots, trunk, and especially roots often contain large amounts
of starch (Keller and Loescher, 1989) and protein (Sauter et al.,
1988), while only trace amounts of soluble carbohydrates are pres-
ent, although poplar may be an exception (Bonicel et al., 1987).
Regarding other potential storage carbohydrates, it is question-
able whether hemicelluloses play any roles as root reserves, despite
work by Priestly (1962) and Kandiah (1979a). Susceptibility of
these compounds to various extraction procedures will vary de-
pending on the development of other crosslinks in the cell walls
(Fry, 1986), which could confound interpretation of a role as storage
compounds. Also, although these extracellular polysaccharides are
known to be secondary carbohydrate reserves in endosperm of cer-
tain seeds (Halmer and Bewley, 1984), other work suggests that
hemicellulose is not a storage material in the grapevine, since its
level is not reduced by acute carbohydrate restriction resulting from
defoliation (Winkler and Williams, 1938). Similarly, defoliation of
apple (Proebsting, 1925) and severe topping of pecan (Smith et al.,
1939) depleted starch, but not hemicellulose, leading these authors
to conclude that hemicellulose was primarily structural in nature.
Location of carbohydrate reserves
The whole tree may be considered a storage organ, and storage
carbohydrates are commonly found in all the perennial parts of the
tree. Temperate trees follow a standard pattern of deposition and
use of these carbohydrates throughout the plant and over the season
(Kramer and Kozlowski, 1979). For example, deposition of starch,
the primary nonstructural root storage carbohydrate, begins throughout
the plant shortly after leaf expansion and usually reaches a peak
after shoot growth ceases in maple (Wargo, 1979), ash (Seybold,
1969), poplar (Isebrands and Nelson, 1983; Nelson and Dickson,
1981), and mulberry (Yamashita, 1984, 1986). Starch deposition
occurs primarily in roots after fruit ripening in apple (Faby and
Naumann, 1986a; Kandiah, 1979a), sweet cherry (Keller and
Loescher, 1989), and pecan (Smith et al., 1986).
For some deciduous fruit tree and vine crops, seasonal changes
in nonstructural carbohydrates have been extensively characterized,
especially in apple (Beattie, 1948; Chong, 1971; Chong and Taper,
1971a, 1971b; Grochowska, 1973; Hansen, 1967; Hansen and
Grauslund, 1973; Hooker, 1920; Kandiah, 1979, 1979b; Loescher
et al., 1982; Mochizuki and Hanada, 1956; Murneek, 1933; Priest-
ley, 1960, 1964, 1981; Proebsting, 1925; Rao and Berry, 1940;
Taper and Liu, 1969; Traub, 1927; Whetter and Taper, 1963) and
in grape (Bains et al., 1981; Eifert and Eifert, 1963; Kliewer, 1965;
Kliewer, 1967; Kliewer and Nassar, 1966; Marutyan, 1962; Pickett
and Cowart, 1941; Scholefield et al., 1978; Winkler, 1929; Winkler
and Williams, 1938; Winkler and Williams, 1945). Other species
studied include peach (Breen, 1975; Dowler and King, 1966; Lash-
een and Chaplin, 1977; Rohrbach and Luepschen, 1968; Rom and
Ferree, 1985; Ryugo and Davis, 1959; Stassen et al., 1981), pear
(Cameron, 1923; Gardner, 1929), pecan (Davis and Sparks, 1974;
Smith and Waugh, 1938; Worley, 1973, 1979); persimmon (Archer,
1941); pistachio (Crane and Al-Shalan, 1977; Crane et al., 1976);
plum (Breen, 1975; De Villiers and Meynhardt, 1972); prune (Braun
et al., 1971; Davis, 1931), sour cherry (Anderson and Hooker,
1927); sweet cherry (Fischer, 1891; Beres, 1972; Keller and Loescher,
1989; Roper et al., 1988); and walnut (Ryugo et al., 1980). Un-
fortunately, roots have not always been considered, but these studies
demonstrate the dynamic nature of nonstructural carbohydrates in
most permanent parts of deciduous plants throughout the year. Gen-
erally, as growth resumes in the spring, carbohydrate reserves are
depleted in shoots and roots, usually beginning before budbreak.
After reaching a minimum, most tissues usually begin to accumulate
reserves immediately. In some cases, this accumulation is inter-
rupted during the period of fruit ripening (Roper et al., 1988). Total
nonstructural carbohydrates (TNC) later reach a maximum at the
time of leaf abscission. TNC remain unchanged or slowly decrease
during the winter, after which the cycle repeats. The data for sweet
cherry are just one example, and seasonal changes in TNC are
shown in Fig. 1 (from Keller and Loescher, 1989).
As in other woody plants, the focus in various fruit crops has
been on above-ground parts, where shoot bark tissues usually con-
tain more soluble carbohydrates than wood, and where starch is
most abundant in the wood (Crane and Al-Shalen, 1977; Crane et
al., 1976; Dowler and King, 1966; Gardner, 1929; Kliewer, 1967;
Proebsting, 1925). During the winter, although the totals may change
only slightly, there may be considerable interconversion of starch
and soluble carbohydrates, especially in shoot bark and wood tissues
(Nelson and Dickson, 1981; Sauter, 1988), but not in roots (Keller
and Loescher, 1989). Apple bark usually contains higher levels of
total nonstructural carbohydrates than wood, but the total tree dry
weight of wood exceeds that of bark, resulting in about equal amounts
of these in bark and wood (Kandiah, 1979a). In sweet cherry, how-
ever, trunk wood, especially that more than several years old, con-
tains few reserves in comparison to other above-ground tissues (Fig.
1). Consequently, the relative importance of trunk and shoot wood
and bark varies with the species.
Although the whole tree may be involved in storage, evidence
that roots play a special role is unclear. Nonetheless, regardless of
species or flowering and fruiting behavior, the root system nearly
always contains higher concentrations of nonstructural carbohy-
drates than any other portion of the tree, and therefore has been
considered the main site of carbohydrate storage. Several kinds of
data support this conclusion for apple (Abusrewil et al., 1983; Chong,
1971; Lockwood and Sparks, 1978a; Murneek, 1933; Priestley,
1960; Priestley, 1964), but seasonal studies of carbohydrate re-
sources showed that the distribution between above- and below-
ground apple tissues remained constant, even though the total amount
in the tree fluctuated. This and other similar data for apples have
led to the conclusion that the root system should not be regarded
as a special storage organ (Priestley, 1960; Tromp, 1983). Sup-
porting this contention,
≈70%
of the apple tree’s dry weight may
be in above-ground parts, and, although the concentrations are lower,
these contain almost twice as much extractable carbohydrate on a
whole-plant basis as below-ground parts (Priestley, 1960).
Nonetheless, seasonal changes in root carbohydrates in sweet
cherries and other species suggest that roots play a distinct role in
storage. Keller and Loescher (1989) have shown not only that root
carbohydrate reserves are higher than in other storage tissues (total-
ling 20% or more of root dry weight), but also that root reserves
do not substantially decrease until budbreak (Fig. 1). In contrast to
roots, above-ground sweet cherry tissues begin to deplete carbo-
hydrates in late winter, especially those nearest active sinks. Ac-
cumulation patterns also show that minimum carbohydrate content
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275
of sweet cherry roots did not occur until after storage had begun in
stem tissues (Fig. 1). Similar results were observed in grape (Wink-
ler and Williams, 1945) and sugar maple (Wargo, 1979). Such
differences in the use of root reserves may simply be due to prox-
imity to active sinks (Kramer and Kozlowski, 1979), or reflect the
effects of low soil temperatures early in the growing season.
McCamant (1988) has, for example, shown that use of sweet cherry
root reserves is highly temperature-dependent, with little or no de-
crease in these reserves at temperatures < 10C.
Environmental, developmental, and management effects on
root reserves
An alternative approach to identifying the specific role(s) of root
reserves is to look at responses to environmental, developmental,
and management factors. Unfortunately, responses to environmental
stresses can be complex. For example, slight or transient droughts,
not completely inhibitory to photosynthesis, may inhibit shoot growth,
and, through reallocation of photosynthates, actually increase car-
bohydrate reserves (Bradford and Hsiao, 1982). Other stresses may
have similar effects (Wagner and Evans, 1985). We have found
similar results in sweet cherry, where deficit irrigation had little
effect on photosynthesis, but carbohydrate reserves increased, es-
pecially in roots (Rom and Loescher, unpublished data).
Temperature may affect use of reserves in several ways. Respi-
ration is important in the dormant season, even in temperate envi-
ronments, and, because respiration increases exponentially with
temperature, maintenance costs may ultimately affect productivity
(Kramer and Kozlowski, 1979; Waring, 1987). Low temperatures
not only slow respiration, but also influence carbohydrate reserves
qualitatively. For example, high sorbitol levels in tracheal sap of
apple correspond with the lowest temperatures on a monthly or even
a daily basis (Raese et al., 1978; Williams and Raese, 1974; Hansen
and Grauslund, 1973, 1978; Ichiki and Yamaya, 1982). At the same
time, starch decreases in parenchyma cells, suggesting starch-sor-
bitol interconversions. In all these cases, however, sorbitol concen-
tration in apple xylem dropped weeks before budbreak (Williams
and Raese, 1974). Although the timing is different, similar quali-
tative changes have been found in sucrose-translocating trees, e.g.,
sugar maple (Cortes and Sinclair, 1985) and poplar (Sauter and
Kloth, 1987; Sauter, 1988).
In sweet cherry, temperature clearly affected use of root starch
reserves with little or no decline in starch below 10C (McCamant,
1988). Such temperature-dependent declines in root starch were also
correlated with top growth (Fig. 2), and occurred only as long as
growing buds were present (topped or debudded trees showed no
decline). Continued top growth clearly stimulated hydrolysis and
transport of root reserves. This relationship also suggests that use
of root reserves primarily involves transport and not respiration;
otherwise, root starch levels would have also declined at higher
temperatures in the absence of buds or top growth. Although one
study has shown that low root temperatures slow apple shoot growth
and perhaps nitrogen uptake (Tromp and Ovaa, 1984), there are
very few other data on the effects of root temperatures on carbo-
hydrate use and transport in woody plants.
Fruiting often decreases carbohydrate reserves, but there is little
evidence that roots are especially affected in fruit trees. In prune,
for example, starch in bark, wood, spurs, roots, and trunk was
higher in nonbearing trees than bearing ones throughout the year,
except at the time of the first growth flush (Davis, 1931). Starch
decreased just before harvest in 2-year-old bark and wood and spurs
of bearing trees, but to a lesser extent, or not at all, in nonbearing
trees. In apple spurs from nonbearing trees, starch was significantly
higher than in those from bearing trees during the summer months
for 3 consecutive years (Grochowska, 1973). In mandarin, starch
levels in leaves, branches, trunk, and roots were at least twice as
high in nonbearing than bearing trees. The differences were espe-
cially large in roots (Goldschmidt and Golomb, 1982). These and
similar reports (Archer, 1941; Crane and Al-Shalan, 1977; Hooker,
1920; Jones et al., 1970; Lenz and Küntzel, 1974; Ryugo et al.,
1977) indicate that the presence of reproductive sinks decreases
nonstructural carbohydrates stored in all vegetative tissues. Other
studies, however, have shown equal or higher amounts of nonstruc-
tural carbohydrates in tissues of bearing compared to nonbearing
trees (Crane et al., 1976; Smith et al., 1986; Wood and McMeans,
1981). Although fruiting slowed mid-season accumulation of re-
serves in nearly all above-ground tissues of the sweet cherry, there
was no effect on roots, and, by the season’s end, there were no
differences due to fruiting in any tissue (Roper et al., 1988). The
detection of treatment differences in many of these studies may be
due to the way the results are expressed. For example, the per-
centage of sorbitol and sugars in roots of 2-year-old apple trees was
higher in fruiting than nonfruiting trees (Hansen and Grauslund,
1978). But, the total root dry matter of fruiting trees was less than
half that of nonfruiting trees, and hence the total amount of sorbitol
and sugars was less in fruiting tree roots.
Despite the ambiguity of fruiting effects, removal of leaf and
stem reserves through defoliation or pruning suggests a distinct role
for root reserves. That removal of vegetative parts decreases veg-
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etative growth and the potential to produce future vegetative yield
generally seems clear (Cannell, 1985). Summer pruning effects in
apple (Sauré, 1987) and [
14
C]-labeling in autumn in poplar (Ise-
brands and Nelson, 1983) also confirm the importance of autumn
foliage for root growth and that roots gain sink strength as the season
progresses. Late-season defoliation always results in smaller car-
bohydrate reserves, and the roots are the most sensitive storage
organ to such treatment. In sugar maple, for example, late July
defoliation resulted in a root starch content 1% of control, compared
to 10% of control in shoot wood (Gregory and Wargo, 1985). In
pecans, small roots also showed the greatest starch depletion after
September defoliations (Worley, 1979). Regrowth in both these
species can, however, replenish most of the reserves.
In sweet cherries, defoliation clearly reduced root starch reserves
in November after leaf abscission (McCamant, 1988). Sweet cher-
ries defoliated in August had the least amount of starch in all tissues,
while trees defoliated at later dates had higher levels, increasing
with later defoliation dates (Fig. 3). This pattern suggests, like
regrowth in other species, that photosynthesis, even late in the sea-
son, is important for normal starch accumulation. Photosynthesis in
October was surprisingly important, as the root starch of October-
defoliated trees was half that of the controls. As in sugar maple and
pecan, sweet cherry root starch was the reserve most sensitive to
defoliation. In August-defoliated trees, shoot wood starch concen-
trations were twice that of root wood, when normally root wood
has more than twice the starch of the shoots. In October-defoliated
trees, root starch was half the control, but shoot starch of the same
trees was nearly the same as the controls.
Similar defoliation data indicate root reserves are critical to sur-
vival. In sweet cherry, as in sugar maple, early defoliation resulted
in death of the tree the following year, although shoot reserves were
relatively little affected compared to root reserves (Fig. 3). In ad-
dition, 1 month after bloom the following year, August- and Sep-
tember-defoliated sweet cherries had small, yellow leaves and poor
fruit set (McCamant, 1988). October-defoliated trees did not show
deficiencies, but did have smaller leaves and less overall growth.
The yellow leaves on August and September treatments were prob-
ably due to nitrogen deficiencies, such as those documented in
defoliated apple trees (Faby and Naumann, 1986b, 1986c). Some
nitrogen deficiencies are expected, because metabolic nitrogen that
could be remobilized in the leaves and transported to the bark and
roots for storage is lost entirely when leaves are removed before
normal abscission.
Alternatively, inadequate carbohydrate reserves in the roots could
also create nitrogen deficiencies through a lack of carbohydrate
substrates for new root growth. For example, heavy nitrogen fer-
tilization had little effect in increasing the leaf nitrogen content of
apple trees defoliated the previous summer (Faby and Naumann,
1986c). Root growth in pecans is believed to rely entirely upon
reserves for the first 2 months of the growing season (Lockwood
and Sparks, 1978a, 1978b), and defoliation severely inhibits root
growth in apple trees (Head, 1969). Although October-defoliated
sweet cherries did not show the same nutrient deficiencies of trees
defoliated earlier in the season, and yet had less root starch than
the controls, the lack of root reserves could still have been the main
cause of nutrient deficiencies (McCamant, 1988). For example,
Worley (1979) hypothesized a threshold level for reserve carbo-
hydrates in pecans, below which no yield could be expected. A
similar situation may exist in sweet cherry and other species, where
the dramatic differences between early and late defoliation treat-
ments suggest a probable threshold level of reserve carbohydrates
for normal leaf development and nitrogen assimilation.
Radioisotope labeling studies
The best evidence for the role of roots in early season growth
comes from labeling studies. Kandiah (1979b), Quinlan (1969), and
Hansen and Grauslund (1973) all showed that, at budbreak, labeled
carbohydrates from apple roots were translocated to the first formed
leaves and also to flowers (Quinlan, 1969; Hansen and Grauslund,
1973). In pecan, Lockwood and Sparks (1978a, 1978b) found most
of the label from root reserves in the first formed leaves, but also
found the same reserves in leaves formed well after budbreak, as
well as in male and female inflorescences. Similar data have already
been mentioned for grape.
After terminal buds set in the late summer, the flow of photo-
synthates is primarily basipetal, e.g., in grape (Hale and Weaver,
1962), apple (Kandiah, 1979b; Quinlan, 1969), and pecan (Lock-
wood and Sparks, 1978a, 1978b). Such photosynthates are believed
to become structural components (Lockwood and Sparks, 1978a,
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1978b; Hansen and Grauslund, 1973) as well as reserves. Similarly,
in sweet cherry pruned to two branches, with one [
14
C]-labled and
the other unlabeled, although much of the [
14
C]-label went to the
roots, a considerable amount remained in the leaves, wood, and
bark of the labeled branch (McCamant, 1988). Those remaining in
the top, however, were removed in sweet cherry by excising the
labeled branch after leaf abscission and then following the subse-
quent appearance in the unlabeled branch of [
14
C]-label from root
reserves. There was a small amount of [
14
C]-label in the unlabeled
sweet cherry branch during dormancy, but Priestley (1981) also
noted an exchange of carbohydrates between apple roots and shoots
during dormancy. At advanced budswell in sweet cherry, label in-
creased only in the buds, as noted by Lockwood and Sparks (1978a,
1978b) in pecan. Also, like pecan, when the first sweet cherry
leaves expanded, radioactivity increased in both shoot wood and
bark. Although the most [
14
C]-label was in recently expanded leaves
with less in leaves formed at later dates, cherries clearly use root
reserves at budbreak and during early shoot extension.
xylem sap components are apparently actively secreted into the
apoplast (Sauter and Kloth, 1987; McCamant, 1988).
Transport of root carbohydrate reserves
If xylem sap is nutritionally significant in species that have only
low levels of carbohydrates and other compounds, xylem transport
must occur at high rates. Positive xylem pressure may be a factor
in some species, but the most likely means of driving transport
would be transpiration (Sauter and Ambrosius, 1986). Although
transpiration in dormant trees is relatively low, e.g., with a calcu-
lated flow of 26 liters·day
-1
in a 12-m-tall sugar maple (Milburn
and Zimmerman, 1986), a month between the end of low temper-
atures and the onset of budbreak could account for considerable
translocation, especially when considering the high carbohydrate
concentrations before budbreak in sugar maple (Cortes and Sinclair,
1985), or even lower concentrations, as in sweet cherry (Beever,
1969; McCamant, 1988). Given the tremendous transpiration po-
tential of a stone fruit tree in full bloom, transport rates after bud-
break could be much higher. Birch, which blooms in late winter,
clearly transports hexoses in the xylem with a potential of providing
nutrients to the developing tissues at rates that equal or exceed those
provided through the phloem (Sauter and Ambrosius, 1986).
If woody plants use root reserves early in the season, before
budbreak, how then are carbohydrates translocated acropetally from
the roots to the shoots? During the growing season, most carbo-
hydrate translocation occurs within the phloem. Phloem loading is
a temperature-dependent, active process, and sieve elements often
contain occlusions during the winter. Consequently, there is some
question whether the phloem is active in late winter before budbreak
(Evert et al., 1972). Nevertheless, some phloem cells do appear
functional during dormancy, i.e., a thin layer of sieve tubes nearest
the cambium did not contain callose occlusions in their sieve plates
(Evert et al., 1972); Fisher (1983) has shown that phloem transport
actually occurs during the winter at temperatures as low as -30C
in at least three deciduous species (Salix, Tilia, and Acer).
Following early spring growth demands, xylem solute concen-
trations usually become much lower during the growing season (Fig.
4), although apple xylem sap has been reported to containe hor-
mones (Luckwill and Whyte, 1968) and low levels of carbohydrates
following budbreak (Hansen and Grauslund, 1978). Nonetheless,
other data show export in growing woody plants of [
14
C]-labeled
photosynthates, first to roots presumably as carbohydrates via the
phloem and then as amino compounds to mature leaves through the
xylem (Bollard, 1960; Dickson, 1979; Kato, 1981). Thus carbon
circulates in woody plants much as it does in herbaceous plants
(Andrews, 1986; Pate, 1983).
Control of the use of root carbohydrate reserves
An alternative is xylem transport, which has been well-docu-
mented in several herbaceous plants (Andrews, 1986; Pate, 1983).
There is good evidence for early season xylem transport in some
woody plants. Seasonal changes in xylem sap composition have
been studied in many different woody plants, e.g., kiwifruit, Ac-
tinidia (Ferguson, 1980), apple (Williams and Raese, 1974), willow
(Sauter, 1983; Stanislawek et al., 1987), walnut (Ryugo, 1988),
Douglas fir (Pseudotsuga) (Doumas and Zaerr, 1988), and grape
(Hardy, 1969; Hardy and Possingham, 1969). Although compre-
hensive quantification of the xylem sap is rare (Andersen and Brod-
beck, 1989), late-winter and early spring increases in solute content
are common, and the xylem is clearly an important conduit for
translocation of reserve carbohydrates and other materials in grape
(Andersen and Brodbeck, 1989), birch (Sauter and Ambrosius, 1986),
and willow (Sauter, 1983). Evidence for such transport in tree fruits
is limited, although carbohydrate levels in the xylem sap of stone
and pome fruits were first investigated by Anderssen (1929); later,
Beever (1969) looked at carbohydrates in the xylem sap of fruit
trees at budbreak in relation to fungal growth in the wood. There
is also evidence for early spring xylem transport associated with
hydrolysis of root reserves in apple (Hansen and Grauslund, 1978).
Control of carbohydrate mobilization or use in underground or-
gans such as tubers, roots, and bulbs has been extensively studied
only in the tubers of the fructan-storing Jerusalem artichoke (He-
lianthus tuberosus) and the starch-storing potato (Solanum tubero-
sum) (Halmer and Bewley, 1982). There are almost no data on
control of the use of woody plant root reserves. Signals that control
starch hydrolysis have not been considered beyond what controls
normal budbreak. In fact, the relationship between starch hydrolysis
and dormancy is not always clear (Cottignies, 1986). Gibberellins
and cytokinins when sprayed on the tree will cause budbreak, but
we do not know if they also directly stimulate starch breakdown.
Alpha amylase, an enzyme often stimulated by gibberellins, is nor-
mally associated with the rapid breakdown of starch in many plant
species, but has only been cursorily studied in woody perennials
(Schaefer, 1982; Schaefer and Schwarz, 1986).
Starch hydrolysis in sweet cherry roots appears to be hormonally
stimulated (McCamant, 1988). For example, gibberellic acid (GA)
Most evidence for the role of carbohydrates in translocation in
xylem sap comes from work on sugar maple, where sucrose levels
apparently create the rare phenomenon of positive pressure in the
wood, or bleeding sap (Cortes and Sinclair, 1985; Johnson et al.,
1987; Milburn and Zimmerman, 1986). In contrast, in grape, pos-
itive xylem pressures were closely related to amino and organic
acids, and carbohydrates had only a minor role (Andersen and Brod-
beck, 1989). Other studies have shown high xylem carbohydrate
sap concentrations during winter in species as diverse as apple and
willow, but most of these trees do not have bleeding sap. In willow,
very high sucrose levels, 3% to 5% (w/v), in the xylem sap occur
shortly before bloom (Sauter, 1983; Stanislawek et al., 1988). Sim-
ilar patterns of high levels of reducing sugars were found in birch
(Betula pendula) (Sauter and Ambrosius, 1986). Although much
less than in willow or birch, high levels of hexoses (Fig. 4), but
not sorbitol or sucrose, were found in sweet cherry sap before bloom
(McCamant, 1988). Consistent with other transport phenomena,
278
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induced starch hydrolysis in growing roots excised from trees that
had not yet begun budswell, but auxin and cytokinin were appar-
ently ineffective. GA also appeared to increase extractable
α−
am-
ylase activity. Later, following budswell, starch decreased in all
starch treatments regardless of the presence or absence of growth
regulators; induction had apparently already begun before root ex-
cision. Since trees with growing roots did not lose starch, whereas
those with growing buds lost starch every time, the stimulus is most
likely produced in the buds. Powell (1987) has stated that the rest
influence resides in the buds and is transported to the roots. How
this stimulus gets to the roots is unknown. A paradox also arises
because growing roots are believed to be one of the main sources
of gibberellins, while leaf primordia, or the buds, produce auxins
(Davies, 1987). Young (1987) suggested that auxins may mediate
or start gibberellin production and starch breakdown in apple, but
auxins induced no starch hydrolysis in excised cherry roots.
Clearly, resolving the factor(s) involved in the use of root re-
serves is in the future.
Management effects and implications
Summer-pruning effects on carbohydrate reserves have long been
studied (Winkler, 1929) and can be complex (Saure, 1987). Inter-
pretation is complicated by the same kinds of considerations in-
volved in stress effects. Summer pruning is not the same as defoliation,
since the latter predominantly removes photosynthetic sources while
the former, by also removing vegetative sinks, redirects allocation.
Although summer pruning decreases leaf area and carbon fixation
(Mika, 1986; Saure, 1987), it may increase carbohydrate reserves
and other compounds in roots and elsewhere, depending on timing.
Fertilizer management effects on reserves are also complex. Nu-
trient limitations decrease growth, yet commonly result in starch
accumulating in many tissues. Roots clearly function as storage
organs to include nitrogen reserves in woody perennials (Araujo
and Williams, 1988; Faby and Naumann, 1986b, 1986c; Taylor,
1967; Titus and Kang, 1982). Fertilization timing is a major con-
sideration, since root carbohydrate reserves only increase after com-
petition for photosynthates has decreased, e.g., relatively late in a
season, or after top and reproductive growth have ceased. Carbo-
hydrate reserves may, for example, be reduced by defoliation and
summer pruning and increased by nitrogen fertilizer in the autumn
(Tromp, 1983). Presumably, nitrogen prevents onset of dormancy
or increases late-season vigor and photosynthesis. Nitrogen assim-
ilation as an energy-dependent process would also depend on the
availability of carbohydrates in the roots (Radin et al., 1978), again
a late-season phenomenon (see above section on seasonal changes
in reserves). This dependency may explain why the main cultural
factors that influence nitrogen reserves are not only the amount, but
also the time, of nitrogen fertilization (Faby and Naumann, 1985,
1986a, 1986b, 1986c; Tromp, 1983; Weinbaum et al., 1984).
Given that most cultivated deciduous fruit trees are complex ge-
netic systems with rootstocks chosen in many cases for growth
control, nutrient uptake characteristics, and, ultimately, such factors
as fruit quality and yield efficiency (Westwood, 1978), there is
surprisingly little information on root reserves in different root-
stocks. Study of rootstock and scion interactions demonstrated that
certain rootstocks resulted in greater dry weight of both roots and
shoots, but scion effects on the rootstock were complex (Brown et
al., 1985). Further work in this area may clarify the role of root
reserves in rootstock and scion performance.
SUMMARY
In the last century, Hartig (1858) proposed that carbohydrates are
stored in the roots during winter and move to developing tissues
through the wood in the spring. Xylem transport is now accepted
as the major pathway for movement from roots to shoot in most
higher plants, although the data are somewhat limited for fruit trees
and many other woody species. Root reserves not only occur in
concentrations higher than in other tissues, but are also very sen-
sitive to defoliation and other disruptions of photosynthesis, partic-
ularly late in the season following cessation of vegetative growth.
Root reserves have a role as an important and perhaps the major
source of substrates for the subsequent year’s early respiration, growth,
and development. The sensitivity of root reserves to late-season
stresses may disproportionately affect plant performance and yield,
particularly for early flowering and fruiting. The implications of
these and other roles of root reserves, their effects on nutrient uptake
and assimilation, control of their use and transport, and the specific
effects of management practices, are only beginning to be realized.
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