Annals of Botany 106: 215 –222, 2010
doi:10.1093/aob/mcq029, available online at www.aob.oxfordjournals.org
REVIEW: PART OF A HIGHLIGHT SECTION ON PLANT – SOIL INTERACTIONS AT LOW PH
Genetic improvement for phosphorus efficiency in soybean: a radical approach
Xiurong Wang, Xiaolong Yan and Hong Liao*
Laboratory of Plant Nutritional Genetics, Root Biology Center, South China Agricultural University, Guangzhou 510642, China
* For correspondence. E-mail [email protected]
Received: 2 November 2009 Returned for revision: 23 November 2009 Accepted: 22 December 2009 Published electronically: 12 March 2010
† Background Low phosphorus (P) availability is a major constraint to soybean growth and production.
Developing P-efficient soybean varieties that can efficiently utilize native P and added P in the soils would be
a sustainable and economical approach to soybean production.
† Scope This review summarizes the possible mechanisms for P efficiency and genetic strategies to improve
P efficiency in soybean with examples from several case studies. It also highlights potential obstacles and
depicts future perspectives in ‘root breeding’.
† Conclusions This review provides new insights into the mechanisms of P efficiency and breeding strategies for
this trait in soybean. Root biology is a new frontier of plant biology. Substantial efforts are now focusing on
increasing soybean P efficiency through ‘root breeding’. To advance this area, additional collaborations
between plant breeders and physiologists, as well as applied and theoretical research are needed to develop
more soybean varieties with enhanced P efficiency through root modification, which might contribute to
reduced use of P fertilizers, expanding agriculture on low-P soils, and achieving more sustainable agriculture.
Key words: Soybean, genetic improvement, phosphorus efficiency, root breeding.
IN T RO DU C T IO N
Soybean (Glycine max), as an essential source of protein, oil
and micronutrients in human and animal diets, has become
an increasingly important agricultural commodity, with a
steady increase in worldwide annual production due to its
excellent nutritional value and health benefits (Liu, 1997).
Soybean is cultivated in tropical, subtropical and temperate
areas, often on soils low in phosphorus (P) because of intensive erosion, weathering and strong P fixation by free Fe and
Al oxides (Sample et al., 1980; Stevenson, 1986). Therefore,
low P availability is often a major constraint to soybean
growth and production. At the same time, the world is facing
a future shortage of P fertilizer resources, as P fertilizers are
increasing in cost and P ore deposits that can be economically
mined and processed into fertilizer are limited and will eventually be depleted (Yan et al., 2009). Nutrient-efficient
plants are defined as plants which could produce higher
yields per unit of nutrient applied or absorbed compared
with other plants grown under similar agroecological conditions (Fageria et al., 2008). Therefore, P-efficient varieties
should play a major role in increasing soybean yield.
Developing P-efficient soybean varieties that can efficiently
utilize native P and added P in the soils, which are often in
forms unavailable to plants, would be a sustainable and economical approach to soybean production. This review discusses
the possible mechanisms for P efficiency and genetic strategies
to improve P efficiency in soybean through root-based
approaches. These studies might help scientists to gain new
insights into the mechanisms of P efficiency and genetic strategies for better P efficiency in soybean, particularly through
root modification.
PO S S I B L E M E C H A N I S M S FOR P H O S P H O R U S
EFFICIENCY
Many studies have demonstrated that there is substantial genetic
variation for plant P efficiency. In soybean, our laboratory has
identified P-efficient varieties that grow much better than standard varieties under P-deficient conditions in acid soils, where
the concentration of available soil P is often lower than
20 mg kg21, and show similar yields to standard varieties in
P-fertilized soils (Fig. 1). There are a number of potential adaptive mechanisms that P-efficient plants can employ for better
growth on low-P soils, including changes in root morphology
and architecture, root symbiosis, activation of high-affinity phosphate (Pi) transporters, enhancement of internal phosphatase
activity, and secretion of organic acids and phosphatases into
the rhizosphere (Fig. 2; Raghothama, 1999; Vance et al., 2003;
Gahoonia and Nielsen, 2004a). Therefore, it would be preferable
to identify and select the specific traits that are directly related to
P efficiency and can be modified. These specific traits could be
used for more efficient screening in controlled environments,
or tagged with the molecular markers and then improved
through marker-assisted selection or gene transformation (Yan,
2005). Among the possibly beneficial traits for P efficiency,
some studies have shown that root morphology and architecture,
root symbiosis and root exudates were the most important traits
for efficient P acquisition in soybean (Wang et al., 2004, 2009;
Zhao et al., 2004; Cheng et al., 2008; Liu et al., 2008a).
Root morphology and architecture
Root morphology refers to the surface features of a single
root axis as an organ, including characteristics of the epidermis
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Wang et al. — Genetic improvement for P efficiency in soybean
HC2 (P-efficient)
HC2 (P-efficient)
BD2 (P-inefficient)
BD2 (P-inefficient)
Low P
High P
F I G . 1. Genetic variation for phosphorus efficiency in soybean. Two soybean varieties contrasting in P efficiency were grown on a P-deficient acid soil with or
without P addition. Low P is no P added, high P is 160 kg P ha21 added as triple sulfate phosphorus (TSP). The available P content of the tested soil was
12.60 mg kg21 ( photo by X. Yan).
[P]
Root morphology
Root architecture
Root symbiosis
Pi transporter
Root exudates etc.
Absorb less P
Absorb more P
P-efficient genotype
P-inefficient genotype
F I G . 2. Schematic representation of a number of adaptive mechanisms for better soybean growth on low-P soils.
such as root hairs, root diameter, root cap, the pattern of
appearance of daughter roots, undulations of the root axis
and cortical senescence (Lynch, 1995). Important root developmental processes, such as root hair formation, primary
root growth and lateral root formation, are particularly sensitive to changes in the internal and external concentration of
nutrients (López-Bucio et al., 2002, 2003). Root morphological features, particularly root hairs, are important for plant P
uptake from the soil by expanding the absorptive surface
area of the root and increasing the soil volume explored by
the roots. Studies with many species have shown a significant
correlation between radius, number and length of root hairs
and P influx in plants, indicating a close relationship
between root hairs and P uptake from the soils (Foehse
et al., 1991; Yan et al., 2004). In barley, genotypic variations
in root hairs can significantly affect P uptake from the soil and
grain yields in low-P fields (Gahoonia and Nielsen, 1997,
2004b). This also appears to be the case with soybean. In a
study with two contrasting soybean genotypes and their
F9-derived recombinant inbred lines (RILs), Wang et al.
(2004) found that root hair traits, including root hair density,
average root hair length and root hair length per unit root,
varied significantly among different genetic materials and
that these variations were highly associated with P status in
Wang et al. — Genetic improvement for P efficiency in soybean
soybean plants. However, the root hair traits are possibly
controlled by quantitative trait loci (QTLs) and therefore can
be subject to significant environmental influence.
Root system architecture, the spatial configuration of a root
system in the soil, is used to describe the shape and structure of
root systems (de Dorlodot et al., 2007). Plant root architecture,
or the spatial configuration of roots in the soil, determines to a
great extent the soil volume explored by the roots, and thus is
very important to plant P acquisition in many crop species
studied, particularly in legumes (Lynch, 1995; Liao et al.,
2001a; Zhao et al., 2004). In common bean, comparative
analysis of different genotypes contrasting in adaptation to
low P availability suggested that root architectural parameters,
including lateral root branching, and length and growth angle
of basal roots, and root growth plasticity were related to P efficiency (Lynch and van Beem, 1993; Lynch and Beebe, 1995;
Lynch 1998; Liao et al., 2001b). In soybean, a study employing an ‘applied core collection’ of soybean germplasm provided the first evidence for a close relationship between root
architecture and P efficiency (Zhao et al., 2004). Their study
found that plants with shallow root architecture had better
spatial configuration in the higher-P cultivated soil surface
layer and thus had higher P efficiency and yield.
Interestingly, there seems to be a co-evolutionary pattern
among shoot type, root architecture and P efficiency. Bush cultivated soybean plants have shallower root architecture and
greater P efficiency, and climbing wild soybean plants have
deeper root architecture and lower P efficiency, while the
root architecture and P efficiency of semi-wild soybean lines
are intermediate between cultivated and wild soybean
(Fig. 3; Zhao et al., 2004). The co-evolutionary relationship
between root architecture and P efficiency might be attributed
to the higher nutrient availability in topsoil. A recent field
study further indicated that root architecture and morphology
were closely related to plant P efficiency (Liu et al., 2008b).
Genotypes with shallower root architecture were found to
have optimal three-dimensional root configurations and
longer total root lengths, thus having higher P efficiency and
seed yield under low P conditions. Root plasticity of genotypes
217
with either deep or shallow root architecture was lower than
those with intermediate root architecture, indicating that root
architecture was more stable in the former two groups under
low P conditions (Liu et al., 2008b).
Using suppression subtractive hybridization, Guo et al.
(2008) constructed several low-P induced cDNA libraries
from both P-efficient and P-inefficient soybean genotypes to
identify Pi starvation-induced genes in soybean. The results
showed that of 2000 clones, 210 genes were differentially
expressed in roots and shoots of soybean seedlings under Pi
starvation. Among them, a novel soybean b-expansin gene,
GmEXPB2, was cloned and characterized from a Pi
starvation-induced soybean cDNA library. The results from
both transgenic soybean hairy roots carrying the promoter
of GmEXPB2 and transgenic GmEXPB2-overexpressing
Arabidopsis lines verified that this gene was strongly induced
by Pi starvation, and that this induction was closely related
to primary and lateral root elongation, which led to improved
growth performance and P efficiency compared with control
hairy roots or wild-type plants (Guo, 2008).
It is interesting to note that soybean root architecture might
not only affect P efficiency of soybean per se but also affect
N and P nutrition of maize in a soybean-maize intercropping
system (Tang et al., 2005). The shallow-rooted and
P-efficient soybean genotype had significantly greater advantages over the deep-rooted and P-inefficient genotype when
intercropped with maize. The nutrient acquisition efficiency
of the maize plant intercropped with the shallow-rooted
soybean genotype was significantly greater than that intercropped with the deep-rooted soybean genotype, indicating
that soybean root architecture may play an important role in
the maize/soybean intercropping system. Maize has a fibrous
root system, which is generally more deeply distributed than
the basal roots of the tap root system, such as common bean
and soybean. Those soybean genotypes with shallower roots
might be able to take up P from topsoil, and also avoid competition for subsoil P acquisition with maize (Tang et al.,
2005).
Root symbiosis
Cultivar
Semi-wild
Semi
genotype Wild genotype
F I G . 3. Shoot and root architecture of a soybean cultivar, and a semi-wild and
a wild genotype. Plants had been grown in the field for 3 months. The available
P content of the tested soil was 17.30 mg kg21 (photo by X. Yan).
Significant positive nitrogen (N) and P interactions were
found in field-grown soybean, possibly related to genetic attributes of root morphological and nodular traits (Kuang et al.,
2005). Such a positive N and P interaction in the field might
have resulted from better nodulation, longer root length and
shallower root architecture, and these traits could be considered as selection criteria in further breeding programmes
for better nutrient efficiency in legumes. P addition has considerable impact on rhizobium symbiosis and biological N2
fixation of some genotypes by increasing nodule formation
and nitrogenase activity on the upper parts of the roots
(Kuang et al., 2005). This at least in part explains the observations from the above described field experiment and may
imply that selecting soybean genotypes with shallow root
systems would not only increase P-uptake efficiency but also
facilitate biological N2 fixation.
In a recent study with isolated and purified rhizobium strains
from the nodules of two soybean genotypes contrasting in
P efficiency grown on different low-P acid soils with different
218
Wang et al. — Genetic improvement for P efficiency in soybean
soybean cultivation history, Cheng et al. (2008) found that
inoculation with these rhizobial inoculants not only formed
many nodules, but also increased soybean shoot biomass and
yield, and resulted in improved N and P nutrient status.
Improved N status with resulting enhanced root growth
might be the mechanism by which soybean P uptake was
increased in plants inoculated with the effective rhizobium
strains on low-P acid soils. Inoculating with these effective rhizobial inoculants could significantly improve growth, as well
as N and P content of soybean plants on low-P acid soils
(Cheng et al., 2008).
Another beneficial root trait for P efficiency is enhanced
root symbiosis with mycorrhizal fungi, which may both
mobilize insoluble soil P through their exudates and extend
root absorptive area through hyphae. Under low P conditions,
plants often have higher mycorrhizal infection rate and mycorrhizae contribute more to P uptake (Smith, 2002). At the same
time, it is now recognized that plant growth response to arbuscular mycorrhizae (AM) associations (i.e. the ‘mycorrhizal
growth response’, MGR) varies widely among plant species
and even varieties when soil P availability limits growth.
Some plants ‘typically’ show large positive MGR, whereas
others ‘typically’ show no MGR or even negative MGR
(Tawaraya, 2003; Smith and Read, 2008; Smith et al., 2009).
Some studies have clearly demonstrated the beneficial effects
that both indigenous and inoculated AM had on legume
growth and N uptake (Ganry et al., 1985; Ibijbijen et al.,
1996; Chalk et al., 2006). Results from a pot experiment indicated that soybean genotypes differed in their mycorrhizal
infection rate and that there was a significant interaction
between soybean root architecture, soil P availability and
AM colonization (Liu et al., 2008a). The soybean genotypes
with intermediate and deep root architectures had higher infection rates with AM under low P conditions. The P-efficient
soybean genotypes had either better root architecture or
higher AM colonization, indicating that a complementary
relationship between root architecture and AM colonization
might contribute to soybean P efficiency (Liu et al., 2008a).
Root exudates
Low P availability may induce root exudation of a number
of compounds, including organic acids, phosphatases and
other compounds that can mobilize P from bound P pools.
Exudation of organic acids into the rhizosphere has been proposed to increase P availability to the plant by mobilizing the
sparingly soluble mineral P and, possibly, organic P sources
(Dinkelaker et al., 1989; Jones and Darrah, 1994; Johnson
et al., 1996). Cluster ( proteoid) roots in the Proteacea (e.g.
Lupinus albus) can release a large amount of citrate under
P-deficiency conditions, and thus sufficiently increase P nutrition of plants (Dinkelaker et al., 1989; Neumann and
Martinoia, 2002; Kochian et al., 2004). Dong et al. (2004)
showed that soybean genotypes contrasting in P efficiency differed in the type and quantity of organic acids excreted from
the roots under P stress, suggesting that organic acids might
contribute to P uptake in P-efficient genotypes. Further
studies have demonstrated that organic acid exudation was differentially induced by low P and aluminium (Al) toxicity in
soybean plants, with specific induction of oxalate and malate
by low P and citrate by Al toxicity, suggesting different
functions in P efficiency and Al resistance for different
organic acids (Liao et al., 2006). However, the roles of
organic acids supported by in vitro experiments might not
represent the roles of organic acids under real soil conditions.
The reactions of organic acids in soils are extremely complex
(Jones et al., 2003). Once exuded, organic acids can be almost
instantly sorbed to anion exchange sites in acid soils and
rapidly biograded in calcareous soils. Their bioavailability
and effective nutrient mobilizing capacity can therefore be
reduced quickly (Jones and Brassington, 1998; Ström et al.,
2001). In addition, the concentration of organic acids in soil
solution is generally low, ranging from 1 to 50 mM (Strobel,
2001). Even using 10 mM organic acid extractants at pH 7.5,
there was only 1.9 and 0.8 mM P released by citrate and
oxalate, respectively, far below the growth demands for
plants (Ström et al., 2005). Therefore, fundamental research
on organic acids and their interaction with soils still needs to
be done to fully elucidate their roles in soil processes, and
understand the factors controlling organic acid-mediated
nutrient release in different soil types (Jones, 1998; Jones
et al., 2003).
Tian et al. (2003) showed that there were large variations for
leaf acid phosphatase (APase) activity among the tested 274
soybean genotypes with different origins, and APase activity
was generally increased without P fertilizer addition. Also,
the increase in leaf APase activity under low P stress was
mainly due to an increase in the activity of existing isoforms
and not by the induction of new isoforms. The results
suggested that leaf APase activity could serve as an enzymatic
indicator of low P status for soybean plants. Studies with other
crop species demonstrated that APase and phytase secretion
was a major contributor for plant assimilation of organic P
from soils (Li et al., 1997; Hayes et al., 2000; Lung and
Lim, 2006; George and Richardson, 2008). Over-expression
of phytase genes from a soil fungus (Aspergillus sp.) or a
soil bacteria (Bacillus subtilis) in transgenic model plants
(such as Arabidopsis thaliana and Nicotiana tabacum) significantly increased exudation of phytase from plant roots
(Richardson et al., 2001; Mudge et al., 2003; George et al.,
2005; Lung et al., 2005), and several studies have reported
that plant purple APase genes such as MtPHY1 and MtPAP1
were expressed in transgenic Arabidopsis and increased
phytase exudation (Xiao et al., 2005, 2006). At the same
time, results have shown that enhanced exudation of phytase
might not help to improve plant P nutrition due to the low
availability of phytate in the soil (George et al., 2005). Our
studies found that over-expression of an Arabidopsis purple
APase gene (AtPAP15) containing a carrot extracellular targeting peptide not only increased the secretion of APase from
transgenic soybean plants, but also significantly enhanced
intracellular APase activity in leaves, as well as P efficiency
and yield on media of low organic P (Wang et al., 2009).
This suggested that enhanced intracellular APase activity
might be more important for crops to adapt to a wide range
of low P soils.
In addition, root plasma membrane Hþ-ATPase was also
found to be involved in the adaptation of soybean to Pi starvation. P uptake might be regulated in part via modulation
of the activity of plasma membrane Hþ-ATPase under Pi
Wang et al. — Genetic improvement for P efficiency in soybean
219
During the 20th century, conventional breeding produced a
vast number of varieties and hybrids that contributed immensely to higher grain yield, stability of harvests and farm
income (Borlaug, 2000). Conventional breeding also plays an
important role in the selection of new soybean varieties.
Recently, conventional breeding methods (backcross breeding,
recurrent selection, etc.) were employed to develop soybean
varieties with superior root characteristics with a focus on
root architecture and other important agronomic traits that
enable better adaptation to acid soils (Yan et al., 2006).
After being tested under various soil/climatic conditions
through Chinese National Field Trials, seven new soybean varieties have been officially certified by the Chinese Ministry of
Agriculture and now are being released to the farmers in nine
provinces of southern China. These new varieties show substantial yield gains in low-P soils compared with conventional
genotypes. They typically out-performed some local varieties
two- to three-fold in both biomass and grain yield under low
P conditions (Cheng et al., 2010).
study, a population of 106 F9 RILs derived from a cross
between BD2 and BX10, contrasting in both P efficiency
and root architecture, was used for mapping and QTL analysis
(Liang, 2007). Preliminary results indicated that most of the
root traits showed a continuous, normal distribution of phenotypic traits, indicating that these were controlled by QTLs.
Some of the root traits (such as root architecture, total root
length and root surface area) within the populations were positively correlated with P-uptake efficiency of soybean plants.
Some of these root traits had relatively high heritability,
suggesting that these traits can be selected as breeding
indices with large selective potential. Using simple sequence
repeat markers as well as other types of molecular marker,
Liang (2007) have successfully identified a number of QTLs
associated with important root traits and/or P efficiency in
soybean. Studies are underway to employ MAS for further
improvement of P efficiency and other agronomic traits using
the major QTLs identified.
Recently, QTLs controlling P deficiency tolerance using 152
RILs derived from a cross between P-stress-tolerant and
-sensitive parents were mapped by Zhang et al. (2009). Five
agronomic traits, namely shoot dry weight, root dry weight,
total dry weight, P-use efficiency and P-acquisition efficiency,
were used to map the QTLs associated with P efficiency.
Thirty-four additive QTLs and eight pairs of epistatic QTLs
were detected on 12 linkage groups and provided a basis for
fine mapping and cloning of a number of P efficiency genes.
The identified QTLs might be useful in improving the stress
resistance of soybean against a complex nutritional disorder
caused by P deficiency (Zhang et al., 2009). At the same
time, breeders need to take into account the complexity of
QTLs and to test the effects of individual loci in the targeted
genetic background to obtain the expected phenotypes for
the genes of interest (Yu et al., 2002). These markers might
be able to play more direct roles in breeding programmes if
they could be used explain a large portion of the genetic variability associated with P efficiency, and if the expression of the
trait was not greatly affected by genotype –environment
interactions.
Marker-assisted selection
Genetic engineering breeding
The stock of DNA markers has been increasing year by year
in various crop plants (Mackill et al., 1999; Brar, 2002).
Developing strategies for using these markers in practical
breeding has been one of the major research subjects in the
past decade (Ishii and Yonezawa, 2007; Moose and Mumm,
2008). Due to the difficulty in directly measuring root traits
and the significance of genotype –environment interactions,
successful examples of using root-trait QTLs to facilitate
genetic improvement in P efficiency remain scarce. In
common bean, Liao et al. (2004), Beebe et al. (2006) and
Ochoa et al. (2006) used QTL analysis to show the importance
of basal roots and adventitious roots for P acquisition. Yan
et al. (2004) identified multiple QTLs for Hþ exudation, and
root-hair density and length, which were associated with the
QTLs for P efficiency in the field. In soybean, there are few
reports on QTL analysis of P efficiency, and very few QTLs
for root traits related to P efficiency have been identified
(Li et al., 2005; Liang, 2007; Zhang et al., 2009). In one
Conventional breeding programmes have sometimes failed
for genetic reasons, such as sterility, incompatibility and lack
of significant variability, and genetic engineering techniques
have proven useful in overcoming some of these problems
(Oldach et al., 2001; Doebley et al., 2006; Ulukan, 2009). In
recent years, important successes in terms of soybean yield
and quality, herbicide tolerance, pest and disease resistance,
and other agronomic aspects have been achieved via genetic
engineering (Nelson and Renner, 1999; Owen, 2000;
De Ronde et al., 2004; Krishnan, 2005; MacRae et al., 2005;
Pline-Srnic, 2005; Eckert et al., 2006; Tougou et al., 2006;
Manavalan et al., 2009). However, few studies have reported
on improvement of P efficiency in soybean by genetic engineering techniques (Chiera et al., 2004; Wang et al., 2009).
In one study, a transgenic approach was used to alter
soybean seed phytate content by expressing a soybean
phytase gene (GmPhy) during seed development to degrade
accumulating phytic acid (IP6). IP6 levels in transgenic
starvation (Shen et al., 2006). They suggested that
indole-3-acetic acid was involved in signal transduction of Pi
starvation by activating the plasma membrane Hþ-ATPase in
soybean roots (Shen et al., 2006).
RO OT B R E E D I N G S T R AT E G I E S TO I M P ROV E
P H O S P HO R U S E F F I C I E N C Y I N S OY B E A N
Plant breeding is the science of changing the genetics of plants
to increase disease resistance, productivity and product quality
in economically important species. Important techniques
include conventional breeding, marker-assisted selection
(MAS) and genetic engineering via transgenesis. Wide genotypic variation and high hereditability for root morphology
and architecture, root symbiosis and root exudates in
soybean provide opportunities for selection and breeding
P-efficient soybean varieties through root trait selection.
Conventional breeding
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Wang et al. — Genetic improvement for P efficiency in soybean
Control
AtPAP15:OX
F I G . 4. Growth performance of transgenic soybean materials in low-P soils. Control: wild-type soybean; AtPAP15:OX: soybean lines over-expressing AtPAP15.
The available P content of the tested soil was 15.39 mg kg21 (photo by H. Liao).
seeds decreased compared with control soybeans, and ectopic
phytase expression during seed development reduced phytate
content in soybean seeds, which therefore increased P availability in animal diets (Chiera et al., 2004).
In another study, the Arabidopsis purple APase gene PAP15
directed by an extracellular targeting sequence was successfully transformed into soybean (Wang et al., 2009). The transgenic lines exhibited significantly improved plant dry weight
and plant P content when grown on sand culture containing
phytate as the sole P source. Furthermore, the transgenic
lines exhibited improved yields when grown on acid soils
(Fig. 4). This study is the first report of the expression of a
plant APase gene in soybean, which led to a significant
improvement in P efficiency and plant yield (Wang et al.,
2009).
CO N C L US I O N S AN D P E R S P E C T I V E S
The above studies have helped us to gain new insight into the
mechanisms of P efficiency in soybean that could be used in
both the theory and the practice for genetic improvement of
soybean varieties. Once clearly identified, these traits could
be used for more efficient screening in controlled environments, or tagged with molecular markers and then incorporated into other varieties through MAS or transgenic
approaches. Recent progress in plant molecular biology has
provided both opportunities and challenges to plant biology
research, resulting in the emergence of many new areas for
study. Among these, root biology is a new frontier of plant
biology for systematic studies of the many processes involved
in plant nutrient mobilization, uptake, transport and translocation as well as their effects on plant growth, development and
adaptability. Root biology will certainly facilitate the development of P-efficient soybean varieties. Further studies involving
collaborations between plant breeders and physiologists, as
well as additional applied and theoretical research are
needed to develop crop species with enhanced P efficiency
that will contribute to reducing the use of P fertilizers, expanding agriculture on low-P soils and achieving more sustainable
agriculture.
ACK N OW L E DG E M E N T S
We thank our colleagues Drs J. Tian, J. X. Wang and J. Zhao
for helpful discussions and comments. This research was in
part supported by the 7th International Symposium on
Plant – Soil Interactions at Low pH, the National Natural
Science Foundation of China and the McKnight Foundation
Collaborative Crop Research Program.
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