Plant Physiology Preview. Published on May 24, 2011, as DOI:10.1104/pp.111.175414
Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future
crops
Jonathan P. Lynch
Department of Horticulture, Penn State University, University Park, PA, 16802
1. Low soil phosphorus availability is a primary constraint to plant productivity
Plant growth in the vast majority of terrestrial ecosystems is limited by low phosphorus
availability. Over 70 percent of all terrestrial biomass occurs in low phosphorus soils, including
over half of agricultural land (Figure 1). Phosphorus availability is declining in many systems
because of soil degradation, which has affected over half of global agricultural land and 75% of
agricultural land in Africa. Intensive phosphorus fertilization is uncommon in the low-input
agriculture common in poor nations, and has limitations as a long-term strategy because of
limited reserves of high-grade phosphate ore deposits, the energy costs of producing fertilizer,
and the environmental cost associated with intensive fertilization. The development of crops
with greater phosphorus efficiency, defined as the ability to grow and yield in soils with reduced
phosphorus availability, would substantially improve food security in developing nations, while
enhancing the sustainability of agriculture in rich nations (Lynch, 2007).
2. Phosphorus is an immobile soil nutrient
Phosphate is highly immobile in soil, because it reacts with many chemical and
biological soil constituents. Plant strategies to acquire phosphorus are therefore oriented around
two basic themes: 1) soil exploration, and 2) mobilization of phosphate from poorly available
phosphorus pools in the rhizosphere. This update focuses on phenes controlling soil exploration
by roots, since they are subject to selection in crop breeding programs, and since root
deployment is senior to many other root phenes affecting phosphorus acquisition, by
determining the placement of root exudates and symbionts in specific soil domains, and thereby
their functional benefit.
3. Phenes affecting soil exploration for phosphorus acquisition
3.1. Topsoil foraging
Because of the immobility of phosphorus in soil, surface soil strata, enriched by the
deposition of plant residues over time, generally have greater phosphorus availability than
subsoil strata. Root traits that enhance topsoil foraging are therefore important for phosphorus
acquisition. Substantial differences exist in topsoil foraging within and among species.
Architectural traits associated with enhanced topsoil foraging include shallower growth angles of
axial roots, enhanced adventitious rooting, a greater number of axial roots, and greater
dispersion of lateral roots (Figure 2).
Shallower root growth angle
In maize, bean, and soybean, shallower root growth angles (RGA) of axial roots (basal roots
in legumes, seminal and crown roots in maize; Figure 3) increase topsoil foraging and thereby
phosphorus acquisition. To determine the value of genotypic variation in RGA for phosphorus
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acquisition, it is useful to compare plants that have varying RGA but have otherwise similar
phenotypes. Since RGA is controlled by multiple genes, useful tools for this analysis are
Recombinant Inbred Lines (RILs), created by repeated selfing of F2 progeny from parents
contrasting for the phene of interest, resulting in a set of typically 100 or 200 homozygous
inbred lines segregating for RGA yet sharing the same genetic background. RILs are powerful
tools for the analysis of quantitative phenes like RGA since they permit the evaluation of a
phene in an array of related yet distinct genomes. RILs are also useful for identifying genetic loci
associated with phene expression (Quantitative Trait Loci or QTL). Cosegregation of QTL
controlling a phene with phosphorus acquisition is strong evidence that the phene is important
for phosphorus acquisition in a range of phenotypes. Analysis of maize and bean RILs varying
in RGA shows that this phene has a dominant influence on phosphorus acquisition, accounting
for up to 6-fold variation in phosphorus acquisition and 3-fold variation in yield in bean low
phosphorus soil (Lynch and Brown, 2001), and 2-fold variation in phosphorus acquisition in
maize (Zhu et al., 2005). QTL associated with RGA in bean cosegregate with yield under
phosphorus stress (Liao et al., 2004). Functional-structural modeling supports a positive role for
RGA in phosphorus acquisition, showing that in stratified soils shallow RGA increases
phosphorus acquisition by increasing topsoil foraging, and that in soils with uniform phosphorus
distribution shallow RGA improves phosphorus acquisition by reducing competition for
phosphorus among roots of the same plant (Lynch and Brown, 2001). RGA of axial roots is an
important phene for topsoil foraging and phosphorus acquisition in annual crops.
Basal Root Whorl Number
The main structural roots of annual legumes are the primary root emerging from the seed,
and basal roots appearing at the base of the subterranean hypocotyl. In bean, basal roots occur
at distinct nodes or ‘whorls’ along the base of the hypocotyl. Basal root whorl number (BRWN)
varies among genotypes from 1 to 4, with each whorl typically generating 4 basal roots (Figure
4). Uppermost whorls produce roots with shallower RGA, and lower whorls producing roots of
progressively steeper angle. Therefore, greater BRWN may increase soil exploration by
increasing the vertical range of root deployment. In a field study on low phosphorus soil in
Mozambique, RILs with 3 whorls accumulated 60% greater biomass than related RILs with 2
whorls (Miguel, 2011). BRWN appears to be under relatively simple genetic control- 3 QTL
explain 58% of phenotypic variance for BRWN in bean (Miguel, 2011).
Adventitious rooting
Adventitious roots emerging from subterranean shoot tissue may increase phosphorus
acquisition because they typically have shallow RGA and are metabolically cheaper than other
root classes. In bean, adventitious roots have greater specific root length, lower tissue
construction cost, more aerenchyma (see below), and less lateral branching than other axial
roots, which permits them to explore the soil for less metabolical investment (Lynch and Ho,
2005). Bean genotypes with greater adventitious root formation had greater growth and
phosphorus acquisition in low phosphorus soil. However, excessive adventitious rooting may
decrease phosphorus acquisition by diverting carbohydrates from lateral branches of basal
roots, thereby decreasing total soil exploration (Walk et al., 2006). In bean adventitious root
formation is under strong genetic control, with 19 QTL accounting for 19-61% of phenotypic
variation in the field (Ochoa et al., 2006).
Lateral branching
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The formation of lateral roots diverts root foraging from axial elongation and thereby
exploration of new soil domains to root proliferation and soil exploitation near the existing
location of the axial root. Theoretically phosphorus acquisition would be optimized if roots had
reduced lateral branching in low phosphorus soil domains, permitting greater axial elongation,
and greater lateral branching in high phosphorus patches. This is evident in bean and maize, in
which low phosphorus reduces lateral rooting more than it reduces axial elongation (Borch et
al., 1999; Mollier and Pellerin, 1999). In young plants with few axial roots, lateral branching may
increase exploration of soil domains not reached by axial roots. This may account for the
observation that increased lateral rooting among young maize RILs under phosphorus stress
was associated with substantially greater phosphorus accumulation and growth (Zhu and Lynch,
2004). Lateral branching is under complex genetic control in maize, where 15 relatively small
effect QTL have been identified (Zhu et al., 2005). The plasticity of lateral rooting in response to
phosphorus availability is under genetic control, indicating that plasticity is a potential selection
criterion in crop breeding (Zhu et al., 2005).
3.2. Reducing the metabolic cost of soil exploration
The metabolic cost of soil exploration is an important component of plant growth under
low phosphorus availability (Lynch and Ho, 2005). Variation among RILs for root costs is
associated with phosphorus acquisition in maize and bean. Genotypic variation for root costs
may be caused by several types of phenes. Anatomical variation may reduce root respiration by
changing the proportion of active and inactive tissue. Architecture phenes can reduce root costs
by reducing competition for phosphorus within and among plants, and by regulating biomass
allocation to root classes of varying metabolic cost. Morphological phenes such as root hairs
can increase phosphorus acquisition at minimal metabolic expense.
Aerenchyma reduces the metabolic costs of soil exploration
Root cortical aerenchyma (RCA) varies constitutively among genotypes (Figure 5a), and is
induced by suboptimal availability of oxygen, water, N, P, and S. RCA is an important adaptive
response to hypoxia by improving oxygenation of root tissue, and may be generally useful for
soil resource acquisition by converting living cortical tissue to air space, thereby reducing the
nutrient and carbon costs of soil exploration. Genotypes of maize and bean vary in RCA
formation, which in maize is strongly related to root phosphorus content and respiration, and
root growth maintenance in low phosphorus soil (Figure 5b). SimRoot modeling indicates that
RCA could increase growth 70% in maize under phosphorus stress and 14% in bean, primarily
by reducing the phosphorus content of root tissue, and secondarily by reducing root respiration
(Figure 6; Postma and Lynch 2010). RCA formation in maize is under the control of several QTL
accounting for about half of phenotypic variation (Mano et al., 2007).
Root Etiolation
Bean roots under phosphorus stress show reduced secondary development and radial
expansion in favor of continued root elongation, a process called ‘root etiolation’ (Figure 7a).
Bean genotypes with greater root etiolation under phosphorus stress have reduced root
metabolic costs and increased soil exploration (Morrow de la Riva, 2010). SimRoot modeling
indicates that this phene may increase shoot growth by 38% over the first 40 days of growth
under low phosphorus (Figure 7b).
3.3 Root hairs
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It is well established that root hairs are important for phosphorus acquisition by expanding
the effective phosphorus depletion zones around the root. Root hairs are especially important
for phosphorus acquisition in nonmycorrhizal plants, since mycorrhizal hyphae fulfill some of the
same functions as root hairs. However, genotypic variation in root hair length and density is
important for phosphorus acquisition regardless of the mycorrhizal status of the plant (Miguel,
2004). Physiological analysis of wildtype and hairless Arabidopsis genotypes, and contrasting
RILs of maize, indicates that the direct metabolic cost of root hairs is negligible (Lynch and Ho,
2005). Root hair length and density are attractive targets for crop breeding programs because
they vary substantially among genotypes (Figure 8), are directly associated with phosphorus
acquisition regardless of mycorrhizal status (Figure 9), they are under relatively simple genetic
control, and are amenable to direct phenotypic selection (Lynch, 2007). Root hair length and
density in maize and bean are controlled by several QTL, which in bean show cosegregation
with yield in low phosphorus soils (Yan et al., 2004; Zhu et al., 2005).
3.4. Phenology
An important limitation to phosphorus acquisition by roots is the slowness of phosphorus
diffusion to the root and the time required for recharge of solution phosphorus from soil
phosphorus pools. Plants that are able to extend the length of time that roots are deployed in
the soil will benefit by increased phosphorus acquisition as well as increased duration and
therefore utility of acquired phosphorus in plant tissue. Annual plants typically delay flowering
and maturation in response to phosphorus stress. In Arabidopsis, genotypic variation in
phenology, and phenological delays caused by phosphorus stress, were strongly correlated with
phosphorus acquisition (Nord and Lynch 2008). Extending crop phenology, and therefore the
duration of root foraging, may therefore increase phosphorus acquisition in those environments
where temperature or water availability do not curtail reproduction.
4. Phene interactions
The value of a phene for phosphorus acquisition may depend on the expression of other
phenes in the plant phenotype. Such interactions may be synergistic, neutral, or negative. For
example, four distinct phenes associated with root hair phenotypes in Arabidopsis: root hair
length, root hair density, the distance from the root tip to the first appearance of root hairs, and
the pattern of root hair bearing epidermal cells (trichoblasts) among non hair bearing cells
(atrichoblasts), have a combined effect on phosphorus acquisition 371% greater than their
additive effects (Lynch and Ho, 2005). Morphological, anatomical, symbiotic, and biochemical
phenes expressed by root axes should have significant synergies with architectural phenes,
since architectural phenes determine the position of root axes in time and space, and therefore
the soil domain in which spatially localized phenes are expressed. For example, longer root
hairs are twice as beneficial for phosphorus acquisition and plant growth under phosphorus
stress when located on shallow roots as they are when located on deep roots, because of the
greater phosphorus availability in surface soil strata (Miguel, 2011). Similarly, phosphatases
that release phosphorus from organic compounds would be more useful if produced by shallow
roots than by deep roots, since soil organic matter typically decreases with depth. In contrast,
carboxylates capable of releasing phosphorus from Fe and Al oxides may be more useful when
released into deeper soil horizons where these forms of phosphorus predominate. Root
architectural phenes interact by altering the extent of competition within and among plants,
which is an important determinant of phosphorus acquisition (Lynch and Brown, 2008).
Architectural phenes may negatively interact by generating competition for internal resources,
as is evident in the case of abundant adventitious rooting reducing plant phosphorus acquisition
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by reducing assimilate supply to basal root laterals in bean (Walk et al., 2006). Likewise
anatomical phenes that reduce root costs may show positive synergism with architectural traits
by reducing competition for internal resources among roots of the same plant. Our
understanding of such interactions is very limited. The large number of possible phene
interactions in integrated phenotypes (e.g. 10 traits each existing in two states would result in
210 integrated phenotypes) makes simulation modeling an attractive complement to empirical
research.
5. Tradeoffs
Evaluation of the utility of a phene for phosphorus acquisition must consider potential
tradeoffs for other plant processes. Direct tradeoffs for many architectural phenes result from
diversion of internal plant resources from other functions, as is evident in the competition for
assimilates between adventitious and basal root laterals, in which excessive biomass allocation
to one root class diverts resources from another root class, resulting in reduced overall
phosphorus acquisition. Architectural tradeoffs can also result if concentration of foraging effort
in one soil domain reduces exploitation of other soil domains. This is especially important for
phenes related to phosphorus acquisition, since phosphorus availability is greater in surface soil
strata, but water and nitrate are typically located in deep soil strata. Architectural tradeoffs for
phosphorus and water have been demonstrated for RGA in bean, in which shallower genotypes
had superior growth under phosphorus stress, but deep-rooted genotypes had superior growth
under water stress (Ho et al., 2005). The direct and indirect tradeoffs for root phenes related to
phosphorus acquisition are poorly understood. It is likely that the large genotypic variation
observed for most root phenes is related to the diversity of soil environments in which plants
have evolved, as well as tradeoffs associated with specific phenes. A better understanding of
fitness tradeoffs for root phenes is needed for their intelligent deployment in crop breeding
programs.
6. Belowground Competition
Root phenes affecting phosphorus acquisition are also likely to affect plant performance in
competitive environments, such as those confronted by the majority of wild and agricultural
plants. The effects of root phenes on belowground competition may be a direct result of
resource competition for phosphorus, and may also be an indirect result of altered plant growth.
An example of growth-mediated effects of a root phene on competition is the positive effect of
root hairs on plant performance in mixed stands of Arabidopsis at low phosphorus but not at
high phosphorus (Bates and Lynch, 2001). An example of the direct effect of a root phene on
resource competition for phosphorus is the observation that bean genotypes with shallow roots
outcompete genotypes with deep roots in low phosphorus fields, because of enhanced topsoil
exploitation and reduced competition among roots of the same plant (Lynch and Brown,
2008). The effects of root phenes on belowground competition are poorly understood, and
represent a knowledge gap that must be addressed for the informed deployment of root phenes
in crop breeding programs.
7. Deployment of root phenes in crop breeding programs
The development of crop genotypes with enhanced phosphorus acquisition efficiency (PAE)
represents an important opportunity to improve food security in developing nations, where crop
yields are severely limited by low phosphorus availability (Lynch, 2007). Simple screening for
yield in low phosphorus soils has not been an effective breeding strategy to improve PAE,
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because of the confounding effects of spatial variability in phosphorus availability, co-occuring
biotic and abiotic stresses, and the improbability of identifying genotypes possessing useful
phenes in a setting in which the possession of many distinct, yet interacting, phenes is
necessary for organismal success. Furthermore, elite crop germplasm has been subject to
decades of selection with irrigation and fertilizer, meaning that sources of useful root phenes are
more likely to be found in landraces (e.g. Figure 8), which may not have other agronomic
attributes conferring success in field screening, such as disease resistance or high yield
potential. For these reasons, a physiological breeding strategy, targeting the improvement of
specific phenes known to increase phosphorus acquisition, is more likely to be fruitful than
simple yield screening of elite germplasm under phosphorus stress. The prerequisites for this
strategy are 1) identification of the target phene(s), which implies a comprehensive
understanding of how the phene affects crop performance in specific agroecosystems, 2)
sources of genetic variation for the target phenes, 3) phenotyping platforms permitting the
efficient evaluation of phene expression in many genotypes, and 4) an understanding of the
likely effects of improved genotypes on the productivity and sustainability of the agroecosystems
of interest. In cases where these prerequisites are in place, root phenes for phosphorus
acquisition are being employed in crop breeding programs. For example, RGA, root hair length
and density (RHL/D), and BRWN are all being employed as direct phenotypic selection criteria
in bean breeding programs in Central America and Mozambique. In these breeding programs
the use of root phenes as selection criteria has permitted the identification of excellent
germplasm sources for these phenes among otherwise poorly adapted landraces, has enabled
rapid phenotypic screening of young seedlings grown in the lab, and has permitted focused
breeding strategies such as phene introgression into elite lines. New bean lines emerging from
these programs typically have 20-40% greater yield under stress than current cultivars (eg IIAM
2010). New soybean lines possessing root architectural traits for superior phosphorus
acquisition are being deployed in Southern China (Wang et al. 2010). Homology among root
phenes enhancing phosphorus acquisition in common bean, soybean, and maize suggests that
these phenes would have general application in the breeding of annual crops with greater PAE.
Architectural multilines
The development of architectural multilines consisting of closely related genotypes
having contrasting root architecture may offer several advantages over traditional monocultures
for stressful environments. For example, multilines consisting of shallow and deep rooted
genotypes may benefit from reduced interplant competition, and greater yield stability in
environments in which both drought and low soil fertility are important. This hypothesis is
supported by an analysis of architectural multilines of bean grown in stressful environments in
Central America, in which multilines tended to have greater yields than the average yield of their
monoculture components (Henry et al., 2010).
High-throughput phenotyping for root architectural phenes
The precise definition of root phenes controlling phosphorus acquisition greatly
facilitates the development of efficient, high-throughput genotyping platforms. Traits expressed
in young seedlings such as RGA, BRWN, and RHL/D may be directly and easily phenotyped in
growth pouches or roll-ups in the lab (http://roots.psu.edu/). More complex traits expressed
later in plant development such as adventitious root formation are amenable to marker assisted
selection (MAS) using QTL or other molecular markers, although these tools have limited
availability in many developing countries, where the need for phosphorus efficient genotypes is
greatest. A number of important root architectural phenes can be rapidly phenotyped in the field
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using a simple manual method called ‘shovelomics’, in which root crowns are excavated and
visually scored for several root phenes at a rate of 2 min/plot (Trachsel et al., 2010).
Functional structural modeling
In silico analysis of the relationship between specific root phenes and soil resource
acquisition through functional structural modeling is a useful tool to guide crop breeding. As
noted above, simulation models are capable of evaluating a large number of integrated
phenotypes in a large number of soil environments, identifying a subset of potential phenotypes
deserving empirical investigation. Modeling is the only practical way to assess the large number
of phene interactions with other phenes and with environmental variables in integrated
phenotypes, a critical step in defining breeding priorities. Modeling also permits the evaluation of
the utility of specific phenes and integrated phenotypes in future climate scenarios, which is
especially important in the stressful environments of developing nations, which could be
seriously affected by global climate change (St.Clair and Lynch, 2010).
System Impacts
Relatively little is known regarding the effects of phosphorus efficient crop genotypes on
the productivity and sustainability of agroecosystems. However, the available evidence indicates
that these effects should be benign. In rich nations, such genotypes would require less
fertilization, thereby reducing production costs and environmental pollution. In poor nations,
characterized by low-input agriculture, crop genotypes with enhanced phosphorus extraction
from the soil could potentially deplete soil fertility over the long term by ‘soil mining’. In bean,
phosphorus efficient genotypes may actually conserve soil fertility by reducing soil erosion
through the formation of greater canopy biomass (Henry et al., 2010). Phosphorus efficient
legumes may also contribute to soil fertility by enhanced biological nitrogen fixation, which is
quite sensitive to phosphorus supply, and may have greater ability to utilize locally available
phosphorus sources such as rock phosphorus. Economically, the greater productivity of
phosphorus efficient genotypes would permit third world farmers greater flexibility in soil
management options, purchasing fertility inputs, etc., in addition to greater food security and
household income. Therefore it does not appear that deployment of root phenes for enhanced
phosphorus acquisition in crop genotypes will have negative consequences for
agroecosystems.
8. Prospects
The identification of root phenes for enhanced phosphorus acquisition is enabling crop
breeders to develop new genotypes with better yield in low fertility soils of Africa, Asia, and Latin
America. With the advent of high-throughput phenotyping platforms for specific root phenes, it is
now possible to discover the genetic basis of genotypic variation for these phenes, which will
enable the development of more powerful molecular breeding strategies. Significant knowledge
gaps remain in our understanding of the root phenome; how phenes interact to affect the fitness
of integrated phenotypes, how phenes for enhanced phosphorus acquisition may incur tradeoffs
for other plant functions, and how genotypes with improved phosphorus acquisition may affect
the long term productivity of agroecosystems, considering factors such as nutrient cycling,
intercropping, and the socio-economic impacts of improved genotypes on rural communities.
These challenges call for a renewed focus on plant phenes and plant physiology at multiple
levels of organization.
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Figure legends
Figure 1. Map of global soil phosphorus availability. The dominance of red and light gray colors,
indicating suboptimal phosphorus availability for the growth of many plant species, indicates the
importance of phosphorus availability as a primary limitation to plant productivity in terrestrial
environments. From Jaramillo 2011.
Figure 2. Root phenes associated with genotypic differences in adaptation to low phosphorus
From Lynch 2007.
Figure 3. Shallow vs deep basal root growth angles in two common bean (Phaseolus vulgaris
L.) genotypes grown in the field in South Africa.
Figure 4. Variation in Basal Root Whorl Number (BRWN) in common bean (Phaseolus vulgaris
L.) is related to the number of basal roots produced and therefore soil exploration.
Figure 5. 5a: Cross sections of seminal roots of maize (Zea mays L.) showing genotypic
difference in cortical aerenchyma formation, which replaces living cortical cells (left) with airfilled lacunae (right). Genotypes are closely related progeny (recominant inbred lines) of the
same 2 parents. 5b: Maintenance of root growth in a low-P field as related to cortical
aerenchyma formation in unrelated maize (Zea mays L.) genotypes. Root weights are
expressed as the proportion of corresponding high-P roots. Each point is the mean of 4
replicates.
Figure 6. Visualization of the simulated root architecture of common bean (Phaseolus vulgaris
L.) and maize at 40 days after germination. HP=high soil phosphorus (18 μM), LP=low soil
phosphorus (3 μM). HP visualization shows a root system without RCA formation, as the root
system with RCA formation was visually not different. From Postma and Lynch, 2010.
Figure 7. 7a: Root etiolation: reduced secondary development of common bean (Phaseolus
vulgaris L.) roots in response to phosphorus stress. Root cross sections are from tissues of
equivalent age in equivalent root classes of the same genotype. 7b: effect of root etiolation on
shoot biomass accumulation in low phosphorus plants 40 days after germination as modeled in
SimRoot. From Postma and Lynch, unpublished.
Figure 8. Genotypic variation for root hair length and density in common bean (Phaseolus
vulgaris L.). The genotype on the top is the result of scientific breeding and is an important
commercial cultivar in Central America. The genotype on the bottom is a Peruvian landrace.
Figure 9. Longer root hairs improve phosphorus acquisition in the presence and absence of
mycorrhizal inoculation in common bean (Phaseolus vulgaris L.). Plants were grown for 28 days
in low-P soil in pots with (+VAM) or without (-VAM) mycorrhizal inoculum. Genotypes are
recombinant inbred lines having long or short root hairs. Each bar is the mean of 4 replicates,
bars = SEM. From Miguel, 2004.
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Figure legends
Figure 1. Map of global soil phosphorus availability. The dominance of red and light gray colors,
indicating suboptimal phosphorus availability for the growth of many plant species, indicates the
importance of phosphorus availability as a primary limitation to plant productivity in terrestrial
environments. From Jaramillo 2011.
Figure 2. Root phenes associated with genotypic differences in adaptation to low phosphorus From
Lynch 2007.
Figure 3. Shallow vs deep basal root growth angles in two common bean (Phaseolus vulgaris L.)
genotypes grown in the field in South Africa.
Figure 4. Variation in Basal Root Whorl Number (BRWN) in common bean (Phaseolus vulgaris L.) is
related to the number of basal roots produced and therefore soil exploration.
Figure 5. 5a: Cross sections of seminal roots of maize (Zea mays L.) showing genotypic difference in
cortical aerenchyma formation, which replaces living cortical cells (left) with air-filled lacunae (right).
Genotypes are closely related progeny (recominant inbred lines) of the same 2 parents. 5b:
Maintenance of root growth in a low-P field as related to cortical aerenchyma formation in unrelated
maize (Zea mays L.) genotypes. Root weights are expressed as the proportion of corresponding
high-P roots. Each point is the mean of 4 replicates.
Figure 6. Visualization of the simulated root architecture of common bean (Phaseolus vulgaris L.) and
maize at 40 days after germination. HP=high soil phosphorus (18 μM), LP=low soil phosphorus (3
μM). HP visualization shows a root system without RCA formation, as the root system with RCA
formation was visually not different. From Postma and Lynch, 2010.
Figure 7. 7a: Root etiolation: reduced secondary development of common bean (Phaseolus vulgaris
L.) roots in response to phosphorus stress. Root cross sections are from tissues of equivalent age in
equivalent root classes of the same genotype. 7b: effect of root etiolation on shoot biomass
accumulation in low phosphorus plants 40 days after germination as modeled in SimRoot. From
Postma and Lynch, unpublished.
Figure 8. Genotypic variation for root hair length and density in common bean (Phaseolus vulgaris L.).
The genotype on the top is the result of scientific breeding and is an important commercial cultivar in
Central America. The genotype on the bottom is a Peruvian landrace.
Figure 9. Longer root hairs improve phosphorus acquisition in the presence and absence of
mycorrhizal inoculation in common bean (Phaseolus vulgaris L.). Plants were grown for 28 days in
low-P soil in pots with (+VAM) or without (-VAM) mycorrhizal inoculum. Genotypes are recombinant
inbred lines having long or short root hairs. Each bar is the mean of 4 replicates, bars = SEM. From
Miguel, 2004.
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Figure 1
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Figure 2
Non-adapted genotypes
Adapted genotypes
aerenchyma
more adventitious roots
root etiolation
topsoil
shallower basal roots
subsoil
more dispersed laterals
more basal root whorls
mycorrhizas
longer, denser hairs
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more exudates
RCOOH+
phosphatases
Figure 3
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Figure 4
5
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Figure 5
Seminal root weight (LP/HP)
5a
5b
Root porosity under low P (%)
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Figure 6
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Figure 7
7a
7b
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Figure 8
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Figure 9
Phosphorus content (mg/plant)
3.5
3.0
LP+VAM
LP-VAM
2.5
2.0
1.5
1.0
0.5
0.0
G13
G53
G88
G16
long root hairs
G80
D84
short root hairs
Genotype
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