Journal of Experimental Botany, Page 1 of 14
Traits and selection strategies to improve root systems and
water uptake in water-limited wheat crops
A.P. Wasson1, R.A. Richards1, R. Chatrath2, S.C. Misra3, S.V. Sai Prasad, G.J. Rebetzke1, J.A. Kirkegaard1,
J. Christopher5and M. Watt1,*
1CSIRO Plant Industry, GPO Box 1600, Canberra, ACT Australia, 2601
2Directorate of Wheat Research, Karnal, 132 001, India
3Agharkar Research Institute, Agarkar Road, Pune, 411004, India
4Indian Agricultural Research Institute, Regional Wheat Research Station, Indore, 452001, India
5Queenlsand Alliance for Agricultural and Food Innovation, University of Queensland, Leslie Research Centre, PO Box 2282,
Toowoomba Queensland, Australia, 4350
* To whom correspondence should be addressed. E-mail: email@example.com
Received 18 December 2011; Revised 19 March 2012; Accepted 21 March 2012
Wheat yields globally will depend increasingly on good management to conserve rainfall and new varieties that use
water efficiently for grain production. Here we propose an approach for developing new varieties to make better use
of deep stored water. We focus on water-limited wheat production in the summer-dominant rainfall regions of India
and Australia, but the approach is generally applicable to other environments and root-based constraints. Use of
stored deep water is valuable because it is more predictable than variable in-season rainfall and can be measured
prior to sowing. Further, this moisture is converted into grain with twice the efficiently of in-season rainfall since it is
taken up later in crop growth during the grain-filling period when the roots reach deeper layers. We propose that
wheat varieties with a deeper root system, a redistribution of branch root density from the surface to depth, and with
greater radial hydraulic conductivity at depth would have higher yields in rainfed systems where crops rely on deep
water for grain fill. Developing selection systems for mature root system traits is challenging as there are limited
high-throughput phenotyping methods for roots in the field, and there is a risk that traits selected in the lab on
young plants will not translate into mature root system traits in the field. We give an example of a breeding
programme that combines laboratory and field phenotyping with proof of concept evaluation of the trait at the
beginning of the selection programme. This would greatly enhance confidence in a high-throughput laboratory or
field screen, and avoid investment in screens without yield value. This approach requires careful selection of field
sites and years that allow expression of deep roots and increased yield. It also requires careful selection and
crossing of germplasm to allow comparison of root expression among genotypes that are similar for other traits,
especially flowering time and disease and toxicity resistances. Such a programme with field and laboratory
evaluation at the outset will speed up delivery of varieties with improved root systems for higher yield.
Key words: Architecture, drought, genetics, gravitropism, molecular markers, phenotyping, vigour.
Rainfed wheat production in many parts of the world is
dependent on stored soil moisture. Here we explore which
root traits are most likely to be valuable for improving
water uptake to increase yield, and discuss efficient ways to
select for these traits in breeding. This paper defines an
approach to breeding that can be used in any system where
root traits, in conjunction with management, can be used to
overcome environmental constraints on growth. This paper
focuses on selecting for desirable root system traits for
production systems where deep water at the end of the
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season is likely. Examples of relevant production systems
Australia, and southern Africa where water is very limited,
but also ranging to more favourable rainfed systems such as
in Europe where deep soil moisture may also be available.
We note where the traits discussed will be ineffectual or
detrimental in alternative environments.
Plant breeders generally shy away from selection for root
traits as they have a low heritability, and expression varies
with soil type and rainfall (Cooper et al., 1999a, b; Tuberosa
et al., 2002; Malamy, 2005). Plant breeders generally assume
that direct selection for yield will indirectly select varieties
with the optimum root system for delivering the highest
yields. This appears to be the case with maize breeding in
the USA, where annual genetic yield gain of 77 kg ha?1has
been achieved at the optimum plant density for the varieties
grown (Duvick et al., 2004). Modelling suggests that the
narrowing of shoot and root architectures in higher density,
earlier-sown cropping systems underlies yield gains in these
environments, which have relatively high, predictable rain-
fall during the growing season (Hammer et al., 2009). It is
possible that more directed selection for specific root
architecture traits could enhance yields in dryland cropping
regions. Evidence for this comes from modelling studies for
wheat in Australia where it has been shown that selection
for deeper, more effective roots could significantly improve
capture of water and nitrogen (Manschadi et al., 2006;
Asseng and Turner, 2007; Lilley and Kirkegaard, 2011).
Trait-based selection and breeding complements more
empirical breeding approaches for yield. Trait-based selec-
tion has advantages in that it ensures there is appropriate
genetic variation in breeding populations for selection
progress to be made. It is also expected to have advantages
in terms of selection methodologies using molecular
markers. A more complete discussion of the advantages of
trait-based selection is found in Richards et al. (2002, 2010).
Trait-based breeding for root traits is an order of magni-
tude more difficult than for most above-ground traits. To
overcome this, fast laboratory-based selection methods for
root traits need to be developed that are related to
phenotypic expression in the field. Furthermore, it may be
possible to develop a proxy screen of an easily observed and
quantified trait that reflects what is happening below-
ground. Then, if required, molecular markers that account
for a significant proportion of the variability in the root
trait may also be identified and developed from these
screens, and used within breeding.
This paper will focus on root developmental traits. We
recognize, however, that root traits that overcome biotic and
abiotic constraints are critical to maintaining root length,
function, and water capture, and are first order targets in
breeding programmes for rainfed conditions (Passioura,
2006). Organisms that feed on roots, such as fungi, termites,
nematodes, and aphids, severely reduce crop performance in
dry environments by reducing rooting depth and root
proliferation (Audebert et al., 2000). Similarly, toxic levels of
microelements such as aluminium (Kochian, 1995; von
Uexkull and Mutert, 1995) and boron (Jefferies et al., 2000)
rainfall regionsof India,
can restrict root growth. A focused breeding approach has
been successful in overcoming some of these constraints.
Breeding programmes have developed molecular markers for
biotic resistances, such as resistance to cereal cyst nematode
(Ogbonnaya et al., 2001) and root lesion nematode (Williams
et al., 2002), to improve water uptake. Incorporating traits
conferring resistances to toxicities have also improved pro-
ductivity (Tang et al., 2001, 2002; Delhaize et al., 2004;
Munns et al., 2006). Overcoming subsoil constraints by direct
genetic selection for tolerances to physical and chemical
constraints such as extremes in soil strength and density, pH,
salinity, and toxicities allows morphological root traits to
contribute to deep water uptake, and thus are an integral
part of a genetic improvement programme for roots
(Yambao et al., 1992; Passioura, 2006; Botwright Acuna
et al., 2007; Haling et al., 2010).
We also recognize that agronomic practices can greatly
increase storage and conservation of water in a cropping
system, and can improve the health, growth, and function
of the crop, which can significantly interact with root traits
to improve yield (Watt et al., 2005; Hammer et al., 2009;
Passioura and Angus, 2010). Practices that increase the
conservation, storage and access to water are best combined
with new varieties with root traits to capture that water
(Kirkegaard and Hunt 2010).
Contribution of deep soil water extraction to
Wheat production in India and Australia represents a cross-
section of global spring wheat production. High-yielding
irrigated wheat production and low-yielding rainfed wheat
production systems occur in India. In Australia, summer-
dominant rainfall patterns occur in the northeast grading to
winter-dominant patterns in the southeast, with Mediterra-
nean systems in the south and west. Although the focus is
on those regions with summer-dominant rainfall and stored
soil moisture, the value of deep soil water in ameliorating
water deficits is found in many environments including
more favourable environments such as in the UK (Dodd
et al., 2011) where winter wheat predominates.
Many wheat production systems could benefit from
improvement of the storage of soil moisture (through
management) (Hunt and Kirkegaard, 2012) and soil mois-
ture exploitation (through root genetics). There are exam-
ples of this potential in India and Australia. In India, rain
falls almost entirely in the summer, during the monsoon
season when crops such as rice or sorghum are grown or the
land is fallowed. All wheat is grown in the winter when it is
dependent on water stored in soil after the monsoonal rains
plus any supplemental irrigation. ‘Rainfed’ Indian wheat
typically is irrigated once before sowing to allow the crop to
germinate and emerge, and then relies entirely on water
stored in the soil. Today most rainfed wheat in India is in
the Central and Peninsular regions, and accounts for ;30%
of India’s total production with little access to irrigation.
The trend in Indian agriculture is towards less water for
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irrigation, and storing and use of deep water, either summer
rains or irrigation, will become increasingly important.
Most wheat grown in Australia is rainfed. Like India, it is
grown in the winter. In the northeast cropping region, most
rain falls in the summer and wheat relies largely on
moisture stored in the soil after a preceding summer crop
or fallow. In the southeast, rainfall is highly variable in
amount but it is generally evenly distributed through the
year. It is common for water to be stored deep in the soil at
the time of sowing, resulting from the preceding spring and
summer fallow as well as good weed and stubble manage-
ment (Hunt and Kirkegaard, 2012). In the southwest, most
rain falls in the winter during the season, and thus stored
water at sowing is a less important source of water for
wheat, although rapid root growth, deep into the soil during
the season may increase capture of water and nitrogen,
especially in sandy soils (Anderson et al., 1998; Asseng
et al., 2001; Liao et al., 2004, 2006).
The value of targeting the capture of deeper soil moisture
with selected root traits in a breeding programme is 2-fold.
First, the farmer can measure how much soil moisture is
stored and to what depth at the beginning of the season.
Farmers can store water through pre-season practices, such
as choice of pre-season crop, fallow, or irrigation (e.g. when
irrigation water is available or cheaper, in the case of India).
Farmers can then minimize evaporation of that water
through weed and stubble management (Hunt and Kirke-
gaard, 2012). Once stored beyond the evaporation zone, it
becomes a known source of crop water, while the in-season
rainfall is unpredictable at the time of sowing.
The second value of deeper soil moisture is that its uptake
generally coincides with grain development when crops are
vulnerable to terminal drought (Passioura, 1983). Water use
at this time has a very high conversion efficiency into grain
(water-use efficiency) as vegetative growth has finished and
all photosynthate is used for grain growth. Most of the
increase in yield from late season subsoil water use is due to
increases in the harvest index (ratio of grain to shoot
weight) of the crop (Passioura and Angus, 2010). The high
value of deep water was demonstrated in independent
controlled-environment and field studies. A comparative
study of two wheat genotypes, a standard variety (Hartog)
and a deep and more densely rooted variety (Seri), grown in
large root boxes showed that greater root length in deeper
soil layers contributed to increased yield by allowing more
water extraction during grain filling (Manschadi et al.,
2006). Modelling based on the apparent extraction effi-
ciency of the Seri genotype suggested that each additional
millimetre of water extracted after flowering generated an
extra 0.55 t ha?1of grain yield (Manschadi et al., 2006).
Using rainout shelters in the field and drip irrigation, it was
shown that 10 mm of subsoil water absorbed between
depths of 1.35 m and 1.85 m after anthesis would increase
grain yield by 0.62 t ha?1, equating to 59 kg ha?1for every
additional millimetre (Kirkegaard et al., 2007). Hunt and
Kirkegaard (2012) recently re-evaluated the benefit from
stored out-of-season rainfall at 37 sites throughout southern
Australia under modern farming practices and found that it
contributed between 3% and 72% to yield depending on the
soil type and rainfall distribution of the site.
In addition to evidence from direct experiments and
modelling in wheat, empirical studies with different crops
demonstrate the value of deep roots to yield under drought
in the field. Root depth has been positively correlated with
yield in soybean (Cortes and Sinclair, 1986). In rice, benefits
have been shown to accrue from increased root depth even
under water stress (Kamoshita et al., 2002). Also in rice,
maximum root length, root depth, and basal thickness were
correlated with yield in drought conditions (Champoux
et al., 1995; Li et al., 2005). In a study linking traits in the
laboratory with yield under drought in the field, Li et al.
(2005) showed a positive correlation between root depth
and yield in rice.
Root system traits to increase uptake of
stored soil moisture
Traits to increase root system depth and deeper water
uptake are explored below. We cover shoot traits that may
indirectly impact on root traits that access more deep water,
and root traits that could directly increase water uptake
Trait 1. Deeper root systems (see Fig. 1)
One effective approach to increase root depth has been to
increase the time to reach flowering. The duration of root
descent in wheat is approximately related to the duration
from sowing to flowering as downward growth ceases around
the time of flowering and onset of grain development
(Gregory et al., 1978). Time to flowering has been manipu-
lated in Australian breeding programmes by sowing earlier in
the season with varieties containing vernalization and photo-
period genes that extend the pre-flowering period (Richards,
2006). Earlier sowing improves water-use efficiency and root
Richards, 1995; Kirkegaard et al., 2007). Precise knowledge
of wheat vernalization and photoperiod genes allows for
marker-assisted breeding to adjust flowering times and
duration of vegetative growth to maximize root depth and
capture of soil water in a specific region and at a specific
sowing time (Eagles et al., 2011). Variation in post-anthesis
root growth can also have significant effects on grain yield.
Important differences in the spatial distribution of post-
anthesis root growth have been found between wheat
genotypes (Manschadi et al., 2006). Increasing total post-
anthesis root growth would require allocation of more carbon
to roots post-flowering that could come from more green leaf
area, as is possibly the case in the wheat cultivar Seri
(Manschadi et al., 2006; Christopher et al., 2008), or from
increased specific photosynthetic capacity. Alternatively, it
could be possible to increase root length density at depth
without extra carbon input by modifying specific root length.
An increase in root system depth may result from a faster
rate of root system elongation, also referred to as ‘root
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vigour’ (Palta and Watt, 2009), and/or a narrower angle of
descent (discussed below). There are different terms used in
the literature, such as ‘root system descent rate’, ‘root front
velocity’, and ‘penetration rate’; ‘root vigour’ herein refers
to the overall rate of root system elongation, whereas
‘descent rate’ refers specifically to the rate at which
maximum root depth increases. Faster root growth depends
on processes within the root apex that determine cell
division and expansion (Sharp et al., 2004). Genotypes with
these features may be selected in screens that directly
measure the root elongation rate. Root vigour also depends
on photoassimilate and water allocation to root tips for
growth (Boyer et al., 2010), suggesting that manipulation of
shoot growth would provide extra resources to root growth.
In another example of using shoot traits to manipulate root
traits, selection programmes for high shoot vigour have
resulted in lines with more vigorous early root growth (Watt
et al., 2005; Liao et al., 2006). This early root vigour in
small grain cereals may be associated with a deeper root
system in the field (Richards, 1991; Richards et al., 2007).
It is also possible to use shoot tiller number (branch
number) to increase root vigour. In rice and wheat, it is
Fig. 1. Diagram illustrating four traits to increase deeper water uptake. (1) Deep roots to increase the amount of subsoil moisture which
the root system could access. (2) Greater root length density to enable more complete uptake of the soil moisture. (3) Reduced root
length in surface soil. (4) Reduced resistance to water movement from soil to shoot by longer and denser root hairs (4a), decreased radial
resistance to water movement in roots (4b), and increased xylem size to decrease axial resistance to water transport to the shoot (4c).
Figure 4a kindly provided by Rosemary White, CSIRO.
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observed that genotypes with fewer tillers have deeper root
systems (Yoshida et al., 1982) or longer root systems
(Duggan et al., 2005; Richards et al., 2007).
The angle at which roots penetrate the soil may also
relate to root depth. Root angle has been selected in bean
breeding programmes and has resulted in varieties with
shallow root systems to access phosphorus in the surface
soil (Liao et al., 2001; Lynch, 2011; Lynch and Brown,
2001). The angle at which roots emerge from the seed could
be used as a proxy for deep rooting characteristics,
particularly if it reflects an underlying gravitropic tendency
in the root system. The gravitropic tendency could increase
the depth as more root growth is directed to descent and
not spread. Modelling suggests that selection for a narrow
angle in wheat root systems results in deeper root growth
and higher yields (Manschadi et al., 2008). In seedling
screens of 26 Australian wheats, those adapted to drier
environments where water at depth is frequent tended to
have the narrowest horizontal root spread, while those
adapted to Mediterranean conditions where most water for
the crop comes from frequent but low rainfall events during
the season tended to have a wider spread (Manschadi et al.,
2008). However, in another study, no correlation between
wider root angle in seedling screens and higher yield was
found in Australian Mediterranean environments (McDonald,
2010). The root growth angle of Japanese winter wheat
varieties, assessed in controlled environments, was shown to
correlate negatively with the vertical root distribution of
those varieties in the field (Oyanagi and Nakamoto, 1993).
Wild barley, which evolved in water-limited conditions, has
a narrow angular spread when compared with modern
cultivars (Bengough et al., 2004). In summary, evidence
suggests that the angle of early root formation may
determine rooting depth. However, proof of concept in the
field is required in populations where divergent selection has
been practised for root angle, especially given the strong
influence of soil structure on root growth and distribution
at depth (White and Kirkegaard, 2010).
The root tip drives the gravitropic response in an auxin-
dependent mechanism that alters cell elongation. Many
components of the auxin transport pathway are involved
(Swarup and Bennett, 2009). It is less obvious whether the
mechanism for a gravitropic tendency may drive other root
traits, such as increased growth. The rice OsIAA31 mutant
(Nakamura et al., 2006) has defects in gravitropism and
root length, suggesting overlap in the interpretation of the
auxin signal in cell elongation. A strong gravitropic
response may be a marker of the underlying hormonal
control of root depth. The gravitropic response of wheat
seminal roots was shown to be heritable, with the results
suggesting it was under the control of a single dominant
gene (Oyanagi et al., 1991).
Methodologies for the selection of root growth angle
in seedlings have included, in order of increasing sophisti-
cation, germination paper pouches (Liao et al., 2001),
semi-hydroponics (Chen et al., 2011), gel-filled chambers
(Bengough et al., 2004), and three-dimensional gel-based
imaging setups (Iyer-Pascuzzi et al., 2010; Clark et al., 2011).
Trait 2. Increased root length density in medium and
deep soil layers (Fig. 1)
It is estimated that ;1 cm of root is required to extract the
plant-available water from 1 cm3of soil, with sufficient time,
root–soil contact, and hydraulic conductance in the root
(Passioura, 1983). At harvest, crops with insufficient root
length density at depth can leave water behind in deeper soil
layers (Li et al., 2002). Using modelling and historic rainfall
data, Lilley and Kirkegaard (2011) showed that a faster root
descent rate (20%) resulting in deeper roots, coupled with
more efficient subsoil water extraction (20% beneath 0.6 m
depth), would produce mean yield benefits of 0.32 t ha?1in
southern Australian sites which have water from in-season
and stored rainfall, and 0.44 t ha?1in northern Australian
sites, which rely mainly on rainfall stored in the soil from
pre-season summer rains. Direct quantification of the bottom
third of wheat, barley, and triticale root systems in the field
showed that 6% of the roots were axile roots; the remainder
are branch roots (Watt et al., 2008). Where increased depth
increases the volume of soil moisture available for capture,
more length from branches is needed to improve the capture
of that water. Increased branch length arises from more and
longer branch roots caused by the initiation and development
of branch root primordia in the pericycle; faster elongation
rates of those branch roots; and delayed onset of determi-
nacy of the branch root meristems. Assimilate allocation is
presumably the primary determinant of elongation rates and
vigour, as discussed above; whereas the initiation of branch
root development and cessation of elongation are likely to be
controlled by other mechanisms, such as plant hormones.
Hurd (1964) was the first to select directly for root
density in a breeding programme. He studied patterns of
root development in root boxes with clear faces, to identify
a cultivar that displayed this trait under a variety of soil
moisture conditions. He then demonstrated its high yields in
dry seasons in the field (Hurd, 1964).
A number of empirical studies support Hurd’s breeding
efforts for increased root density. Sorghum varieties from
suboptimal environments have a greater degree of branch-
ing (Masi and Maranville, 1998). Soybean cultivars with
greater root density appeared to have increased water
uptake, and soybean cultivars with extensive fibrous root
systems in the surface layers appeared to be more drought
tolerant (Carter et al., 1999; Pantalone et al., 1999). In
upland rice, root depth, density, and number were all
positively correlated with water acquisition (Price et al.,
2002). Even in shallow soils, an emphasis on root length
density in the ‘deeper’ layers can contribute to improved
water uptake. In rice, varieties with increased root length
density in the 35–45 cm layer had improved resistance to
drought (Henry et al., 2011).
However, the value of greater root length density to yield
in dry conditions is variable. In a study of modern and
older wheat varieties in the sand over clay soils of Western
Australia, Siddique et al. (1990) showed that the older
varieties had more root dry matter and root length density
in the top 40 cm of the soil profile, but there was no
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variation for water extraction or water use. They attributed
higher harvest index and water-use efficiency in the grain
amongst modern varieties to a reduction in root dry matter
and a decrease in the root to shoot ratio. However, this
study was also confounded with variation in the duration of
the pre-flowering period. Palta et al. (2011) recently
concluded that root systems with more total root length
were of value in climates that received rain through the
season, but may exhaust stored soil moisture where it was
the sole source of available water, and shoot vigour was
associated with high root vigour.
Trait 3. Reduced root length density in the topsoil (Fig. 1)
In most wheat crops, root length density in the surface
layers is 3–5 cm cm?3and thus, in theory, exceeds that
required to extract crop available water (Passioura, 1983).
Rainfed wheat crops, where limited rainfall is expected in
the latter part of the season, may benefit from a reduction
in topsoil roots. This excess root length may be a carbon
cost to grain, especially if grown towards the end of the
season when carbon is limiting, and rainfall events are short
and evaporate rapidly before root water uptake. On the
other hand, this extra root length density may be critical for
A study in maize suggested that higher density of roots in
the drying soil layers may also be associated with an
increased flux of abscisic acid (ABA) towards the leaves,
retarding transpiration and grain setting (Giuliani et al.,
2005). Similarly, a split-root experiment in rice with flooded
and drought-treated roots showed that stomatal conduc-
tance and transpiration were reduced before there was
a reduction in leaf water potential, an early drought
response associated with increased ABA. Severing the
drought-treated roots led to a recovery in leaf water
potential, suggesting a role for hydraulic signalling medi-
ated by the reduction of hydraulic conductivity through
cavitation (Siopongco et al., 2008). The strength of this
response varies genotypically, with an upland (dry) line
showing reduced ABA signalling and superior recovery to
a lowland (flooded) line (Siopongco et al., 2009). A study in
barley showed that, independent of the amount of water
available to the plant root system, varieties with fewer roots
in drying soil had more leaf growth and less foliar ABA
than those with more roots in drying soil (Martin-Vertedor
and Dodd, 2011). However, foliar ABA may not be the
appropriate measure of this signalling, as pearl millet near
isogenic lines that differed in foliar ABA concentration were
not shown to differ in total water extraction (Kholova et al.,
2010). This root to shoot signalling could be the focus of
breeding efforts to reduce sensitivity.
Roots in the topsoil of older wheat plants are primarily
nodal axile roots and their branches. It may be possible to
redirect them to deeper layers, perhaps by selecting for
narrower angles of growth. Alternatively, selection could be
made against excessive nodal root growth. Abolishing nodal
roots would also reduce associated root length density by
branch roots (Oyanagi et al., 1993, and references therein).
Nodal root formation is under the control of a single gene
in maize, WOX11, a transcription factor that is auxin and
cytokinin inducible (Zhao et al., 2009). However, a cautious
approach should be taken to the extreme manipulation of
nodal roots. The hormonal evidence suggests overlapping
pathways for nodal and branch root development. In
Arabidopsis, WOX-like genes have been shown to play a role
in lateral root initiation, which suggests overlap in the
control pathways for these two types of roots (Deveaux
et al., 2008). Both branch and nodal roots have been shown
to be generated as part of plastic responses to environmen-
tal cues. This suggests that alterations in nodal root
development may have unwanted side effects in branching
in seminal and other earlier nodal axile roots, which may
impede our attempts to improve root density at depth.
Another detrimental side effect of reducing roots in the
topsoil is reducing nutrient uptake, for example immobile
P or Zn, which is valuable when taken up during grain
development. It also increases the chance of severe root
system restriction if a main axis is rotted by a pathogen
such as Rhizoctonia fungi.
Surface roots that respond to frequent small rainfall
events with additional growth may be a valuable trait in
Mediterranean environments (Sadras and Rodriguez, 2007).
The moist soil surface may dry before new roots become
functional, but repeated showers may be captured by an
expanded surface root system. Given the cyclical wetting
and drying that occurs in surface layers, shoot character-
istics that result in more shading of the soil surface, reduce
evaporation, and maintain saturation of the air are likely to
be of value to the growth and function of surface roots
(Rostamza et al., unpublished results). These shoot traits
may and could be more easily selected in the field than root
Trait 4. Decreased resistance to water movement from
soil to root by increasing root hair growth and xylem
diameters (Fig. 1)
Two types of resistance determine the uptake of soil water
by roots: radial resistance, the resistance of water passing
from the soil into the root and to the vasculature; and axial
resistance, the resistance of water passing from the root to
the shoot through the vasculature. The relative contribution
of radial and axial resistances to incomplete soil water
uptake was studied by Rowse and Goodman (1981) who
concluded that radial resistance was a greater determinant
of water uptake that axial resistance.
Richards and Passioura (1989) engaged in the best known
example of the manipulation of a developmental root trait
in wheat; reducing the xylem diameter of seminal axile roots
to increase their axial resistance to water from the root
system to the shoot, so that soil water uptake earlier in the
season was reduced, leaving soil moisture available during
grain filling where it contributed directly to the harvest
index. Yields were improved in years of water stress, but the
reduced xylem diameter did not adversely affect yields when
there was abundant rainfall, as the nodal roots developed to
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exploit the additional rainfall (Richards and Passioura,
1989). By combining high axial resistance at the base of the
root system with lower axial resistance in deeper roots, it
may be possible to delay use of soil water until flowering
and grain development to increase the harvest index, and
exploit more fully water from deeper soil layers.
Incomplete utilization of subsoil water has been attrib-
uted to resistance at the soil–root interface (Passioura,
1991). Root hairs provide a mechanism by which the plant
roots’ contact with the soil can be maximized and the
resistance minimized (Fig. 1). Segal et al. (2008) analysed
water uptake by barley mutants lacking root hairs and
showed that, despite greater branching, the bald roots had
less water uptake and less uptake per unit root length.
White and Kirkegaard (2010) observed and quantified the
location and root–soil contact of deep wheat roots in the
field in an Australian clay soil. They did not grow through
soil uniformly, but instead exploited pores and channels and
contacted the soil through root hairs. Root hairs are
especially noticeable where there is a gap between the root
surface and the soil (Fig. 1), and clearly provide hydraulic
continuity between root and soil. Direct selection for longer
and denser root hairs, or hair development that contacts
soil in gaps and pores, using imaging would be challenging
given the high variability of root hairs in the field, and the
possibility that seedling root hairs in the laboratory are not
the same as hairs on components of mature root systems in
field conditions. Two genes for root hair elongation, RTH1
and RTH3, have been identified in maize, and may be
valuable for genetic improvement (Hochholdinger and
Improving uptake by lowering axial resistance has been
proposed for rice. Nguyen et al. (1997) proposed that
increasing xylem size and lowering axial resistance would
allow for better exploitation of water in deeper soil layers.
This was supported by studies linking root thickness with
drought resistance (Ekanayake et al., 1985) and quantitative
trait loci (QTLs) for basal root thickness with yield in dry
upland, but not wet lowland, cultivation (Champoux et al.,
1995; Li et al., 2005). The correlation of root thickness and
xylem size has been made in rice, but the conclusion that
xylem size contributes to drought resistance could not be
drawn (Yambao et al., 1992).
Applicability of the traits
The traits discussed are likely to be of value in a rainfed
wheat production system with summer-dominant rainfall
and evidence of stored soil moisture, particularly at depth.
However, there may be situations where these traits may
not be beneficial.
The deep root trait and the dense root at depth trait are
likely to be valuable where there is a shortfall of water late
in the growing season, a common occurrence globally. As
discussed earlier, in Mediterranean environments with
frequent in-crop rainfall events, there may be little or no
benefit to deep root systems and they may pose an
additional burden on plant development (Palta et al.,
2011). Similarly, in situations where there is deep drainage,
there may be little stored soil moisture to access.
In environments with particularly shallow soils, deeper
root systems will not be of benefit, and focus should instead
be on better capture of rainfall events (where available),
traits to minimize the impact that water deficit has on plant
transpiration, and traits to meter out the available water
over the entire season (such as reducing xylem size).
Reducing root length density in the topsoil may be
particularly inappropriate in Mediterranean environments,
where shallow roots may increase the capture of in-season
High-throughput techniques for the direct
evaluation of root systems in the field do not
Identifying desirable root phenotypes directly in the field
would be the shortest route to the incorporation of traits of
value in a crop-breeding programme. However, that
approach is blocked by the lack of high-throughput
phenotyping techniques for the field.
Traditional studies have focused on excavation techni-
ques, from which root depth and root length density can be
determined. Trenching is labour intensive and slow (Van
Noordwijk et al., 2000). Many comparisons between
varieties can be made in a day using mechanised soil coring
with core-break counts, which correlate well with washed
root length densities (Drew and Saker, 1980; Bennie et al.,
1987). Core sample processing has also been improved with
automatic washing systems (Smucker et al., 1982; Pallant
et al., 1993), imaging of washed roots with flatbed scanners,
and software packages for analysing the washed images
(French et al., 2009; Le Bot et al., 2010; Lobet et al., 2011).
Minirhizotrons are a non-destructive alternative to exca-
vation techniques, where a transparent tube is inserted into
the ground and root growth abutting the tube is imaged
with a camera that is inserted down the tube (Smit et al.,
2000). Because minirhizotrons are non-destructive, the
operator may monitor root growth and turnover. However,
the roots must first grow against the tube wall, limiting
what can be analysed. Furthermore, the interface of the
tube and soil is an artificial environment for root growth,
which may lead to incorrect assessments of the growth
characteristics of the plant. Minirhizotrons have been
shown to over- and underestimate root length density
depending on the species examined and installation angle
(Bragg et al., 1983; Heeraman and Juma, 1993; Rytter and
Rytter, 2011; Vamerali et al., 2012).
Ground-penetrating radar has been explored as a tech-
nique for root measurement, but resolution limitations
mean that it is likely to be restricted to trees and woody
plants (Zenone et al., 2008). Electrical resistance tomogra-
phy has been applied to mapping soil physical properties in
agricultural systems (Basso et al., 2010) and the exploitation
of soil water by roots in a crop stand (Srayeddin and
Doussan, 2009)—both of which are indirect measures of
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root behaviour. However, electrical resistance, measured
with electrical resistance tomography (ERT), has been
correlated with soil moisture and root biomass for alfalfa
growing in a small container (Amato et al., 2009)—offering
the possibility that it could be used for the in situ detection
of roots in the field.
Electrical capacitance measures of root system size were
pioneered in the late 1970s (Chloupek, 1972, 1977), and
a theoretical basis has been developed (Dalton, 1995).
Capacitance was correlated with root system size in maize
at flowering in the field; however, effective measurement is
strongly dependent on the soil being moist when the
measurements are performed (van Beem et al., 1998). It has
also been employed in the study of tree roots (Ellis et al.,
In the authors’ experience ;50 genotypes, replicated four
times, could be soil cored with a tractor-mounted hydraulic
push press and four people in one day. The distribution of
mature root systems was assessed in 10 cm increments to
a depth of 2 m using core-break counting. Correlation with
a subset of samples that were washed and scanned (;3 d)
was ;0.75. Thus, until non-destructive methods are vali-
dated and made to be more rapid, root distribution and
rooting depth can be reliably assessed rapidly at 2–3 min
per core in the field with a traditional technique such as soil
Laboratory and field proxy screens and their
Trait-based selection programmes for breeding require
selection methods that are high throughput for high
numbers of lines, and that correlate with yield. As
discussed, techniques for rapid direct root phenotyping in
the field are not available, particularly for mature, deep root
systems. Thus, high-throughput screens in the laboratory or
the field for a ‘proxy’ trait must be used. A ‘proxy’ trait is
a shoot or root measurement that is likely to be a conse-
quence of, or correlate with, the desired phenotype. For
example, root angle can be thought of as a proxy for deeper
roots in the field, as can high shoot vigour.
The four traits highlighted above can be selected by proxy
in the laboratory at the seedling stage. However, deeper soil
water is captured by adult plant root systems. Mature root
system traits, such as root depth and increased branching at
depth, are highly dependent on soil and seasonal climatic
factors, and on plant phenological stage. Seedling roots in
the laboratory may not express the developmental features of
mature roots. It is assumed that the genetics that drive the
expression of the proxy trait in the laboratory also drive the
expression of the desired trait in the field, and that this
explains the correlation. This is the major pitfall of
laboratory screens; they rely on measurements in young
plants that may not confer the desired phenotype in the field
An alternative to laboratory screens is to use shoot proxy
measurements in the field to identify varieties with valuable
root systems. The simplest of these is to assess shoot
performance such as shoot biomass, yield, grain weight,
maintenance of green leaf area, etc. Other measurements
could include canopy temperature (CT) measured with an
infrared thermometer or camera allowing selection of
genotypes in the field with cool canopies. A cool canopy
indicates transpiring leaf area and can be an indirect
measure of crop access to water by the root systems,
another proxy trait (Blum et al., 1982, 1989; Garrity and
O’Toole, 1995). CT was used for the remote sensing of
wheat lines with deeper roots, and CT at grain filling
negatively correlated to root dry weight at depth (Lopes
and Reynolds, 2010). However, numerous factors indepen-
dent of root depth may affect CT in a segregating popula-
tion. Ignoring these has led to confusion among breeders on
the utility of screening for CT in breeding populations.
These factors (including biomass, canopy height, and
development) must be considered when selecting for geno-
types producing cooler canopies (Rebetzke et al., 2012). The
isotopic signature of carbon in the grain may also be
a valuable indicator of differences in access to water by
mature root systems (Araus et al., 2003). Genotypes with
roots that access more deep water and maintain photosyn-
thetic leaf area and stomatal conductance during grain
filling will generate grain with a different ratio of13C to12C
from those that rely on carbon fixed earlier in the season or
carbon fixed by a plant under drought stress and with a low
stomatal conductance. However, as for CT above, the use
of grain12C/13C discrimination relies on good understand-
ing of tested populations and assumes no confounding of
genotypic differences in anthesis biomass, pre-anthesis
water use, and remobilization of stem carbohydrates
(Condon et al., 2002; Rebetzke et al., 2008).
The major pitfall of indirect field proxy screens is that the
shoot measurements or soil water measurements can be
greatly influenced by the field site and weather in the year of
testing. Imagine a field screen for root systems (depicted in
Fig. 2) where yield measurements are used as an indirect
screen for root depth (not dissimilar from the assumption
that yield breeding produces the variety with the optimal
root system). The plant on the right has a shallow root
system, but one that is fully functional. It has limited
capacity for water uptake (at depth) and delivers the lowest
yield (depicted here as a single head). The plant in the
middle has an improved root system, which is fully
functional. This is the highest yielding variety; having an
optimized root system it has the best water uptake for the
investment in the root system. The variety on the left is the
most unusual; a genetic alteration has caused its roots to
develop with exceptional depth and density. This plant
possesses a trait that we imagine an ‘ideal’ plant could
possess. However, some other physiological constraint
(perhaps insufficient hydraulic demand in the shoots, or
insufficient xylem capacity) renders this deeper root system
non-functional. The variety is, in our hypothetical system,
only capable of taking up the same amount of water as the
variety in the middle, but the energetic demands of its larger
root system result in a lower yield in our screen.
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Some may argue that the middle variety has the superior
genetics, because its root system is optimized. However, the
alternative view is that the variety on the left has the
superior root genetics. Why? Because, superior root systems
may not confer superior yields upon a variety where
a physiological constraint outside of the root system limits
the root system’s contribution to yield.
Thus, the use of indirect screening within trait breeding
should be considered with caution. Trait breeding is based
upon the identification of lines that posses that trait ideal.
However, if the ideal does not have a functional impact on
the proxy trait, then ideotype identification will not occur.
The value of the trait is in the genetics that confer the trait
and the particular environment and year in which it is being
A selection programme with laboratory and
field measurements at the start to identify
a worthwhile proxy screen and develop
varieties to increase deep water uptake and
Here we propose a programme with laboratory and field
measurements in parallel in search of a worthwhile proxy at
the outset of the trait-breeding programme (Fig. 3), to
establish a screen that confers deeper roots with greater
water uptake and yield, and speed up development of a new
variety. This ensures that large investment is not made in
a screen that does not confer a field advantage. Ideally,
a laboratory screen could be identified. This would be much
quicker and more reliable than the field proxy screen as
multiple generations could be advanced annually. The
parallel laboratory and field measurements at the outset
greatly help to build confidence in a laboratory proxy
screen, which, as mentioned above, generally relies on
a seedling trait that may not necessarily translate to mature
root system depth and deep water uptake.
The basis of this programme is the definition of a specific
target environment, the constraints in those environments,
and the rational selection of trait combinations that are
likely to overcome any specific constraints (see section
‘Applicability of traits’). This potentially reduces any
genotype3environment (G 3E) interaction that may limit
Critical in this programme is the selection of the appropri-
ate field environments and management practices, to corre-
late the proxy trait with deep roots, deep water uptake, and
yield. The expression of the trait is expected to be greatly
influenced by the specific field conditions encountered and so
management of these proxies and interpretation of the
response is very important. Field site knowledge, weather
measurement, and consistent management practices ensure
Fig. 2. Cartoon illustrating the problems of reliance on indirect measures of root growth. The plant on the left has the best root traits
(here imagined to be deep, highly branched roots), but an unrelated root or shoot constraint negates the advantage. The non-functional
roots are an energetic burden on the plant. Hence, in an indirect screen, the plant on the left will not perform as well as the plant in the
middle, which has a completely functional root system, even though it does not have the superior root trait (the deep highly branched
roots). The middle plant will, however, out-perform the plant on the right on the basis of superior, functional, root traits.
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that deep water is present, and help to stabilize the field
environment year to year and to avoid the pitfalls highlighted
in Fig. 2.
At the outset, laboratory and field proxy traits for the
ideotype root trait are conceptually identified (Fig. 3). These
are developed and evaluated between the laboratory and the
field, looking for high repeatability, low G3E, high
heritability, and cost-effectiveness (high numbers of lines
with low growing and measurement costs). Most impor-
tantly, any laboratory proxy screens must be expressed in
the field through to maturity and confer the desired trait,
for example deeper roots with greater deep water uptake.
Once the effective screen is developed, germplasm is
screened to identify a donor of the trait. This may be from
a diverse, global selection, biased with old and current high-
yielding lines from environments with deep water to
maximize diversity in the proxy. Alternatively, there may
be a single genotype as a source of the trait already
identified from field evidence and controlled environment
studies, such as in the case of Seri, which was intensively
studied in large root boxes (Manschadi et al., 2006). The
best germplasm to start with, provided it has wide diversity
for the proxy trait, is a mapping population because the
trait can be linked to a genomic region for marker
development. Also mapping populations are comprised of
sister lines and will therefore share a common ancestry. This
reduces the risk of the pitfalls of Fig. 2, where field
expression of the proxy can be masked by genetic differ-
ences in processes that have a large effect on water use such
as disease resistance and flowering time. The genes from the
donor parent of the trait are progressed through a backcross
programme to develop a commercial cultivar with the trait
and other desirable characteristics for yield, including
disease resistances and quality (Fig. 4). In this scheme,
progeny are enriched for the trait with the screen or
a marker for the trait, and those that contrast for
expression of the proxy trait (e.g. ‘tails’) can be evaluated
in the field, to continue to build confidence in the trait. This
is done from the outset, and year to year as the sister lines
become more genetically similar. This ensures that the
proxy correlates adequately with the desirable trait. If the
proxy trait fails at any stage it can be abandoned before
further costs are incurred. It also ensures that diversity in
the ideotype is being incorporated in the selection of the
source trait, and that the ideotype trait is being inherited
through the breeding programme for the proxy trait. It also
allows an early evaluation of the contribution of the trait to
performance, and the identification of any constraints on
the translation of the trait to performance. The approach
should more rapidly lead to material with valuable root
traits, especially if the pitfalls of proxy screening discussed
above are minimized.
Fig. 3. A selection programme with laboratory and field measure-
ments at the start to identify a worthwhile proxy screen and
develop varieties to increase deep water uptake and yield.
Fig. 4. Backcross breeding scheme for selection of germplasm
with a desirable phenotype. This scheme is followed after an
effective screen for the trait has been identified and the best donor
of the trait has been identified (see Fig. 3). The scheme allows
incorporation of desirable yield traits from Parent 2 at the initial
cross, enrichment of lines carrying the desirable phenotype with
the phenotypic screen or marker, validation of the trait value in the
field at (1) and (2), and identification of a desirable line for
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A review of the evidence has shown the considerable value
of stored soil moisture to wheat crops in many environ-
ments and suggests an ideotype breeding approach to
optimize exploitation of this resource. Four traits have been
proposed to improve productivity where this resource is
available: deeper root systems, increased root density at
depth, decreased root density at the surface, and decreased
resistance to the movement of water from soil to roots
through an increase in root hairs and/or xylem diameters.
None of the field-based methodologies reviewed is suffi-
ciently high throughput for a root-breeding programme.
Indirect ‘proxy’ traits are argued to be problematic in an
ideotype breeding approach, so a programme of repeated
revalidation of these traits against direct, low-throughput,
measurements in the field is advocated. This approach can
be utilized in other breeding programmes. The key steps are
the identification of the root-based constraints on pro-
ductivity in a specific target environment, the identification
of ideotype traits to overcome this constraint, and a breed-
ing programme, continuously validated in the target envi-
ronment. Laboratory and field research ‘talk to each other’
from the outset.
The authors are grateful to the Australian Centre for In-
ternational Agricultural Research (ACIAR) and the Indian
Council for Agricultural Research (ICAR) for funding to
develop new wheats with deeper roots.
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