Annals of Botany 112: 317 –330, 2013
doi:10.1093/aob/mcs231, available online at www.aob.oxfordjournals.org
VIEWPOINT: PART OF A SPECIAL ISSUE ON MATCHING ROOTS TO THEIR ENVIRONMENT
A conceptual model of root hair ideotypes for future agricultural environments:
what combination of traits should be targeted to cope with limited P availability?
L. K. Brown, T. S. George*, L. X. Dupuy and P. J. White
The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
* For correspondence. E-mail [email protected]
Received: 12 July 2012 Revision requested: 10 September 2012 Accepted: 21 September 2012 Published electronically: 20 November 2012
† Background Phosphorus (P) often limits crop production and is frequently applied as fertilizer; however, supplies of quality rock phosphate for fertilizer production are diminishing. Plants have evolved many mechanisms
to increase their P acquisition, and an understanding of these traits could result in improved long-term sustainability of agriculture. This Viewpoint focuses on the potential benefits of root hairs to sustainable production.
† Scope First the various root-related traits that could be deployed to improve agricultural sustainability are catalogued, and their potential costs and benefits to the plant are discussed. A novel mathematical model describing
the effects of length, density and longevity of root hairs on P acquisition is developed, and the relative benefits of
these three root-hair traits to plant P nutrition are calculated. Insights from this model are combined with experimental data to assess the relative benefits of a range of root hair ideotypes for sustainability of agriculture.
† Conclusions A cost–benefit analysis of root traits suggests that root hairs have the greatest potential for P acquisition relative to their cost of production. The novel modelling of root hair development indicates that the
greatest gains in P-uptake efficiency are likely to be made through increased length and longevity of root
hairs rather than by increasing their density. Synthesizing this information with that from published experiments
we formulate six potential ideotypes to improve crop P acquisition. These combine appropriate root hair phenotypes with architectural, anatomical and biochemical traits, such that more root-hair zones are produced in surface
soils, where P resources are found, on roots which are metabolically cheap to construct and maintain, and that
release more P-mobilizing exudates. These ideotypes could be used to inform breeding programmes to
enhance agricultural sustainability.
Key words: Arabidopsis, barley, Hordeum vulgare, cost/benefit, modelling, phosphorus, root architecture, root
anatomy, root function, root hairs.
T H E G LOB A L PROB L E M
With the global population set to hit nine billion by 2050 and
the resources needed to sustain this population diminishing,
unsustainable agronomic practices and environmental change
have brought us to the point where a revolution in agricultural
production is necessary to ensure future agricultural sustainability and food security. This second green revolution must
focus on crops which are tolerant to and productive in lowfertility environments and gains need to be achieved across a
range of crops (Lynch, 2007). A new generation of crops
adapted to low/reduced input systems will not only enable
people in some of the poorest parts of the world to provide
themselves with adequate nutritious food and save some products for trade, but will also have a vital part to play in the
high-input systems of the developed world by reducing
inputs and their associated economic and environmental
costs. The key to breeding these crops is the utilization of
the large genetic variation in yield that has been identified in
low-fertility environments. Of the traits responsible for this
yield variation those associated with roots are perceived to
have the most potential to deliver crops for the second green
revolution and by looking below ground we might make the
enormous strides necessary to improve yields to feed nine
billion people (Lynch, 2007; Tester and Langridge, 2010;
Gregory and George, 2011).
One of the most important inputs to agricultural systems is
phosphorus (P) and the issues associated with P bioavailability and acquisition by plants represent problems of
global proportions (Stutter et al., 2012). Phosphorus is an essential nutrient required for plant growth and reproduction
(White and Brown, 2010), but due to its strong reaction with
soil and subsequent lack of mobility it is estimated that
30– 40 % of the world’s arable land is limited by P bioavailability (Runge-Metzger, 1995). In particular, P bioavailability
in the acidic, weathered soils of the tropics and subtropics
represents a major limitation to agricultural production
(Sanchez et al., 1997). The application of P fertilizers is
usually employed to increase soil P bioavailability; however,
this is increasingly problematic (White et al., 2012). While
this is a common solution in the intensively managed agricultural systems of the developed world, it is often impossible in
subsistence agriculture (Sanchez et al., 1997). Furthermore, in
intensive systems up to 80 % of applied P can become immobilized in the soil through the processes of precipitation and
adsorption (Jones, 1998), forcing farmers to apply up to five
times the P fertilizer required by the crop and resulting in P
loading of agricultural soils. In addition, huge quantities of
nutrient-rich manure is often spread on soil resulting in
soluble Pi (inorganic phosphate) levels which often exceed
# The Author 2012. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
For Permissions, please email: [email protected]
318
Brown et al. — Root hair ideotypes for future agroecosystems
the crop requirement (Mikkelsen, 2000). Run-off from such
land is a primary factor in the eutrophication and hypoxia of
lakes and marine estuaries of the developed world (Tiessen,
2008; White and Hammond, 2009). Crucially, the long term
sustainability of applying P fertilizers is also highly questionable with world reserves of high-quality rock phosphate, from
which they are derived, depleting rapidly (Vance et al., 2003;
Dawson and Hilton, 2011). Rock phosphate is now becoming a
strategic material for many countries (Gilbert, 2009). The
availability of P fertilizer also has serious implications for subsistence agriculture in the tropics and subtropics where the majority of the earth’s population live. Here, lack of fertilizer
infrastructure, finance and transport mean that P fertilization
is not a viable option for many of these areas (Sanchez
et al., 1997). There is much scope for improving the utilization
by plants of P that has accumulated in soils, and in the efficiency by which they utilize recently applied fertilizers
(Cordell et al., 2009; Stutter et al., 2012; White et al.,
2012). The global significance of these issues means that the
efficient use of P reserves has become a high priority from a
scientific, political and environmental perspective.
We believe it is possible to tackle some of these issues by
making better use, in agriculture, of traits exhibited by
plants to cope with P deficiency in nature and, thereby,
develop crops for reduced-input agricultural systems.
P L A N T S T R AT E G I E S TO OV E R CO M E
P - D E F I C I T : B E N E F IT S A N D CO S T S
The physiological state of a P-deficient plant is quite specific
and the response to P starvation is multigenic. For example,
the expression of over 1000 genes changes upon P starvation
in arabidopsis (Hammond et al., 2003; Morcuende et al.,
2007).
Plants have evolved two broad strategies for P use in
nutrient-limiting environments – conservation and active acquisition strategies (White and Hammond, 2008; Veneklaas
et al., 2012). Conservation strategies aim to reduce plant P requirement through physiological adjustments which reprioritize internal P-utilization and include reduced growth rates,
remobilization of vacuolar P, reduction in nucleic acid pools,
the use of P-sparing metabolic pathways; and the replacement
of phospholipids with glycolopids and sulpholipids (Vance
et al., 2003, Ticconi and Abel, 2004; White and Hammond,
2008; Veneklaas et al., 2012). Conservation processes enable
plants to maintain their growth when P bioavailability is
low. These strategies are complemented by strategies enabling
plants to acquire P more effectively when P bioavailability is
low. Under conditions of P starvation, plants exhibit increased
root : shoot biomass ratio (Lynch and Beebe, 1995; Hermans
et al., 2006), altered root architecture (Lopez-Bucio et al.,
2000; Williamson et al., 2001; White et al., 2005), increased
lateral rooting and long root hairs (Bates and Lynch, 1996;
Hammond et al., 2009). Also high-affinity P transporters are
more abundant (Mudge et al., 2002; Smith et al., 2003) and
organic acids and phosphatases are synthesized and secreted
(Li et al., 2002). The focus of the second green revolution
should be P-acquisition strategies, since it is the acquisition
of P that will ultimately limit crop production in many cases.
The costs and benefits of the various P-acquisition mechanisms available to plant can be measured both metabolically
and ecologically and their optimization is dependent on environmental factors (Lynch and Ho, 2005). These are summarized in Table 1, which provides us with a way of
rationalizing which of the range of strategies employed by
plants should be targeted for development in future crop
germplasm.
Modifications to root architecture
Under conditions of P deficiency plants allocate more
photosynthate to root production thereby promoting root
growth and allowing the root system to explore greater
volumes of soil for P (Nielsen et al., 2001). The advantages
of this have been demonstrated, for example, in bean
(Phaseolus vulgaris) where genotypes with highly branched,
actively growing, root systems have been shown to be more
P efficient than genotypes lacking such root traits (Lynch
and Beebe, 1995; Lynch and Brown, 2001). This has also
been confirmed in brassicas (Hammond et al., 2009) and
demonstrated for production of lateral roots (Zhu and Lynch,
2004). However, a number of studies have demonstrated that
the increased respiratory burden of a larger root system can
be detrimental to plant growth (Van der Werf et al., 1992;
Snapp and Lynch, 1996; Nielsen et al., 1998, 2001).
Root classes have been shown to differ in their metabolic
costs and the development of adventitious roots has been
shown to be favoured in P-deficient environments in several
plant species (Miller et al., 2003). Biomass allocation to the
production of adventitious roots allows root exploration of
new soil at a reduced carbon cost compared with other root
classes due to their greater specific root length and smaller
linear construction cost (Zobel, 1992; Miller et al., 2003).
Other advantages of adventitious roots include shallow
growth, rapid radial dispersion from the shoot, dispersed
lateral branching, abundant aerenchyma and proliferation of
root hairs. With the greatest concentrations of P typically
found in the top few centimetres of a soil profile, P acquisition
will be favoured in plants with a large proportion of their roots
in the topsoil (Lynch and Brown, 2001). However, plants with
a proliferation of surface roots are prone to both drought and
waterlogging (Simpson and Pinkerton, 1989; Ho et al., 2004).
The heterogeneous distribution of P in the soil is best
exploited by plants exhibiting morphological plasticity of
their root system which allows them to proliferate in
nutrient-rich patches (Hodge, 2004; Robinson, 2005).
Root-system plasticity is an important mechanism to compensate for the large proportion of roots that do not acquire P, provided it does not lead to inter-root competition and increased
metabolic cost per unit P acquired (Ge et al., 2000; Rubio
et al., 2001).
The formation of cluster roots is considered to be one of the
most effective plant adaptations to increase P acquisition
(Lamont, 2003). These root structures are made up of zones
of tightly packed, short rootlets covered in a dense mat of
root hairs which are very effective in mobilizing and taking
up P from the soil. A number of P-mobilizing mechanisms
are concentrated in cluster roots (Keerthisinghe et al., 1998)
into a small volume of soil increasing the surface area of the
TA B L E 1. Summary of costs and benefits of the various P-acquisition mechanisms available to plants
Root traits increasing
P acquisition
Benefits
Costs
Key references
(1) Architectural
Increased
agravitropic growth
Greater volume exploited
Exploitation of P-rich patches; exploitation of P-rich topsoil
Exploitation of P-rich patches
Exploitation of P-rich topsoil at lower carbon cost
Greater volume exploited at lower carbon cost, exploitation of narrower soil
pores, greater plasticity in response, greater dispersion of exudates, rhizosheath
formation
Exploitation of P-rich topsoil
(2) Anatomical
Increased specific
Greater volume exploited per unit carbon cost
root length
Production of
Reduced metabolic expense, improved oxygen availability
aerenchyma
(3) Biological and biochemical
Exudation of organic
anions
Greater P availability from inorganic sources, increased microbial biomass and
altered microbial communities to benefit plant
Exudation of
phosphatases
Increases P availability from organic sources, increased microbial biomass and
altered microbial communities to benefit plants
Rhizosphere
acidification
Greater P availablity from inorganic sources, increased microbial biomass and
altered microbial communities to benefit plants
Associations with
AM fungi
Greater volume exploited beyond the root, exploitation of narrower soil pores,
plasticity of foraging responses, greater P availability through exudation of
fungal organic acids and phosphatases, increased microbial biomass and altered
microbial communities
Greater P availability from inorganic and organic sources through
P-solubilizing and mineralizing micro-organisms, increased microbial biomass
and altered microbial communities to benefit plants
Associations with
specific microbes
Reduced photosynthesis, increased metabolic burden per unit
photosynthesis
Increased construction and metabolic costs, increased competition
between roots, roots in topsoil prone to dehydration and waterlogging
Increased construction costs, high metabolic demand
Increased construction and metabolic costs, roots in topsoil prone to
dehydration and waterlogging
Metabolically cheap to construct, but potential increased susceptibility
to soil pathogens and increased competition between roots
Roots in topsoil prone to dehydration and waterlogging, increased
competition between roots
10, 48
13, 14, 24, 25, 36
20, 47
13, 23, 29, 42
1, 3, 6, 15, 18, 23,
24, 26, 27, 30, 33,
50
13, 24, 37, 49
Reduced resistance to biotic stresses
4, 24, 49
Reduced physical strength, reduced radial transport, fewer niches for
AM fungal colonization
5, 22, 23, 24, 26,
44, 45
Increased metabolic costs, increased microbial biomass and altered
microbial population increasing resource competition with microbes
and/or other negative impacts for plants
Increased metabolic costs, increased microbial biomass and altered
microbial population increasing resource competition with microbes
and/or other negative impacts for plants
Potential increase in metabolic costs, increased microbial biomass and
altered microbial population increasing resource competition with
microbes and/or other negative impacts for plants
Large carbon costs for maintenance of the AM-fungal association,
altered microbial biomass and communities with negative impacts for
plants
7, 17, 19, 26, 31,
34, 39, 40
Increased microbial biomass and altered microbial population increasing
resource competition with microbes and/or other negative impacts for
plants
8, 9, 21, 34, 46
11, 12
16, 31, 32, 38, 43
Brown et al. — Root hair ideotypes for future agroecosystems
Increased root : shoot
ratio
Production of lateral
roots
Production of cluster
roots
Production of
adventititious roots
Production of root
hairs
2, 28, 31, 35, 41
References: 1, Barber (1995); 2, Barea et al. (2005); 3, Brown et al. (2012); 4, Eissenstat (1992); 5, Fan et al. (2003);6, Gahoonia and Neilsen (2004); 7, Gardner et al. (1983); 8, George et al.
(2002); 9, George et al. (2005a),; 10, Hermans et al. (2006); 11, Hinsinger (2001); 12, Hinsinger et al. (2009); 13, Ho et al. (2004); 14, Hodge (2004); 15 Hood and Shew (1997); 16, Jakobsen et al.
(2005); 17, Jones (1998); 18, Jungk (2001); 19, Kirk et al. (1999); 20, Lambers et al. (2006); 21, Li et al. (2003); 22, Lu et al. (1999); 23, Lynch (2011); 24, Lynch (2007); 25, Lynch and Brown
(2001); 26, Lynch and Ho (2005); 27, Ma et al. (2001b; 28, Marschner et al. (2008); 29, Miller et al. (2003); 30, Moreno-Espindola et al. (2007); 31, Morgan et al. (2005); 32, Nielsen et al. (1998); 33,
Raghothama (2005); 34, Richardson et al. (2009a); 35, Richardson et al. (2009b); 36, Robinson (2005); 37, Rubio et al. (2001); 38, Ryan and Graham (2002); 39, Ryan et al. (2001); 40, Ryan et al.
(2009); 41, Seeling and Zasoski (1993); 42, Simpson and Pinkerton (1989); 43, Smith and Read (2008); 44, Striker et al. (2006); 45, Striker et al. (2007); 46, Tarafder and Jungk (1987); 47, Vance
et al. (2003); 48, White and Hammond (2008); 49, White et al. (2005); 50, Zhu et al. (2010).
319
320
Brown et al. — Root hair ideotypes for future agroecosystems
root system and releasing organic anions and acid phosphatases in an exudative burst (Vance et al., 2003). This strategy
for P acquisition is employed by only a very few species which
tend to inhabit soils with extremely low P availability, which is
possibly indicative of the high metabolic input required.
Indeed, it is estimated that half the photosynthetic carbohydrate production of a plant might be required for growth, respiration and exudate production by cluster roots (Lambers
et al., 2006).
Another modification to root-system architecture that
improves P acquisition is the production of root hairs and
this is often concurrent with increases in the root : shoot
ratio. Under P-deficient conditions, root hairs can be responsible for up to 90 % of the P acquired by plants, and, in
many species, root hairs can contribute almost 70 % of the
total surface area of roots (Raghothama, 2005). Root hairs increase the volume of soil explored by roots, access soil pores
otherwise inaccessible to the plant (Misra et al., 1988),
allow dispersion of root exudates (Ryan et al., 2001) and are
implicit in rhizosheath formation (Moreno-Espindola et al.,
2007). Modifications to root hair morphology are considered
to be the cheapest way by which a plant can increase the
surface area of the root system (Bates and Lynch, 2000), but
the observed plasticity of this trait could be indicative of a significant metabolic cost or a biological cost in the form of
increased susceptibility to pathogens (Hood and Shew, 1997;
Zhu et al., 2010).
Modification to root anatomy
A number of anatomical changes can occur in plant roots in
response to P deficiency, including the reduction of root diameter or the production of finer roots (Eissenstat et al., 2000;
Forde and Lorenzo, 2001). An increase in specific root
length, or length of root per mass, enables a plant to
produce longer roots per unit of dry matter (Hill et al.,
2006), and can be achieved either by reducing root mass
density (Fitter, 1985) or by decreasing root diameter.
However, greater specific root length has been linked with
greater vulnerability to biotic stress (Eissenstat, 1992) and
reduced elongation rates and ability to penetrate hard soils.
Another anatomical adaptation to reduce the metabolic cost
of roots is the formation of aerenchyma in response to P starvation (Fan et al., 2003). The formation of aerenchyma
reduces root costs by replacing metabolically active cortical
cells with air spaces, thereby increasing the proportion of
root mass occupied by non-respiring tissues. The reduced
carbon costs associated with replacement of cortical cells by
aerenchyma accompanied by the additional P resources made
available to the plant through the senescence of cortical cell
tissue benefits the P-economy of the plant and contribute to
physiological P-utilization efficiency (Lynch and Brown,
1998; Lu et al., 1999; Koide et al., 2000; Fan et al., 2003).
The costs of forming aerenchyma are unknown, but might
include reduction in niches for colonization by arbuscular
mycorrhizal (AM) fungi, reduced radial transport of water
and nutrients and reduced resistance to physical stresses (Fan
et al., 2003; Striker et al., 2006, 2007).
Modification to the chemistry and biology of the rhizosphere
The manipulation of rhizosphere biochemistry by plants
offers an opportunity to increase P bioavailability (Lynch and
Ho, 2005). Phosphorus bioavailability can be increased
through the acidification of the rhizosphere, the exudation of
organic acid anions and the secretion of extracellular phosphatases (Richardson et al., 2009a). Rhizosphere acidification is
thought to increase P bioavailability by altering the solubility
of inorganic phosphate salts or by affecting P absorption/desorption reactions in the soil (Hinsinger, 2001). While this process
can benefit plant P acquisition in alkaline soils, excess acidification of the rhizosphere can result in reducing P availability and
can lead to aluminium toxicity in acid soils (Ryan et al.,
2001). It has also been demonstrated that alkalinization and
the uptake of calcium ions by plant roots can lead to increased
P availability in the rhizosphere (Devau et al., 2010, 2011).
The importance of organic anions for the P nutrition of plants
has been reviewed by Ryan et al. (2001) and Lynch and Ho
(2005). These compounds are thought to increase P bioavailability by complexing or chelating cations and, thereby, solubilizing
inorganic phosphates, by replacing phosphate on sorption sites in
the soil and by altering the surface characteristics of soil particles
(Bar-Yosef, 1991; Jones and Darrah, 1994; Jones, 1998; Ryan
et al., 2001). Organic anions also increase the availability of P
from organic compounds by facilitating their mineralization by
phosphatases (George et al., 2005a). However, exudation of
carbon in the form of organic anions can be metabolically expensive, in some cases representing over half the below-ground
carbon allocation (Gardner et al., 1983; Dinkelaker et al., 1989;
Johnson et al., 1996a, b; Kirk et al., 1999; Nguyen, 2003). In addition, the short residence time of these compounds in the soil
means their effectiveness may be limited (Marschner and
Romheld, 1996; Gahoonia and Nielsen, 2003).
The secretion of enzymes into the rhizosphere is another important mechanism by which plants can increase P bioavailability. Organic P (Po) forms a substantial component of soil
P (Turner et al., 2002), but before this P becomes available
to the plant it must be mineralized by phosphatases (Tarafdar
and Jungk, 1987; George et al., 2002; Li et al., 2003). There
is significant genotypic variation in exuded phosphatases
both between and within plant species (George et al., 2008).
However, while this variation is related to the ability of
plants to utilize specific organic-P substrates in vitro, similar
relationships are not always found when plants are grown in
soils (George et al., 2005a, 2008).
Mycorrhizal associations are considered to be of great importance in increasing the ability of the host plant to increase
its P acquisition (Clark and Zeto, 2000; Smith et al., 2003;
Morgan et al., 2005; Smith and Read, 2008). The main
benefit to the plant is thought to be the increased volume of
soil that can be exploited through the fungal mycelium
which projects beyond the P-depletion zone of the root
(Smith and Read, 2008). The speed that P moves through
fungal mycelia is faster than P diffusion through the soil,
resulting in rapid movement of P from the soil to the plant
(Smith and Read, 2008). Mycorrhizal relationships have also
been demonstrated to increase the utilization of soil organic
P by plants and to enhance the exploitation of nutrient-rich
patches (Feng et al., 2003). A lack of mycorrhizal colonization
Brown et al. — Root hair ideotypes for future agroecosystems
in species with cluster roots and reduced mycorrhizal colonization in plants with adequate P status, along with strong correlations between plant P acquisition and root traits like root-hair
length and root shallowness in the presence of mycorrhizas
might indicate that mycorrhizal foraging is costly in comparison with root foraging alone (Neumann and Martinoia, 2002;
Brown et al., 2012; L. K. Brown, T. S. George, G. E.
Barrett, S. McLaren, S. F. Hubbard and P. J. White,
unpubl.). Indeed, mycorrhizal associations incur a substantial
metabolic cost to the plant (Koch and Johnston, 1984;
Douds et al., 1988; Jakobsen and Rosendahl, 1990;
Eissenstat et al., 1993; Peng et al., 1993; Harris and Paul,
1997; Nielsen et al., 1998) which in some cases can be nonbeneficial or even parasitic to the plant (Ryan and Graham,
2002; Morgan et al., 2005).
Other associations with soil microorganisms can enhance P
uptake both directly, by increasing P acquisition through the
stimulation of root growth (Jakobsen et al., 2005) and indirectly,
by providing a source of P which contributes to plant P nutrition
(Richardson, 1994). The microbial mass releases phytohormones which can lead to increased root branching and root
hair development (Pitts et al., 1998), thereby increasing the
surface area of the roots in contact with the soil and the opportunity for roots to take up available P. Microorganisms play an
important role in the transfer of P between different organic and
inorganic forms through the processes of solubilization and mineralization (Helal and Dressler, 1989; Perrot et al., 1990;
Seeling and Zasoski, 1993; Macklon et al., 1997; Rodriguez
et al., 1999; Jones et al., 2003; Vance et al., 2003; Hammond
et al., 2004). Moreover, microorganisms contribute significantly
both to the pool of organic anions and to phosphatase activity in
the rhizosphere (Richardson, 1994) and there is evidence that
phosphatases derived from fungal sources are more efficient
in mineralizing soil organic P than those secreted by plants
(Tarafdar et al., 2001). In addition, turnover of the microbial
biomass makes P available to the plant indirectly (Oehl et al.,
2001) and while microorganisms could be seen to be in competition with plants for available P in the short term (McLaughlin
et al., 1988), this subsequent release of P into the rhizosphere
provides a direct source of P for plants in the longer term.
POT E N T IA L TO M A N I P U L AT E ROOT A N D
R HI Z OS P HE R E T RA IT S
Mutants with allelic variation and/or altered expression of
genes affecting P acquisition through root traits have been generated. For example, transgenic plants that secrete microbial
phytases into the rhizosphere have the potential to release P
from inositol phosphates and show enhanced growth and P nutrition when inositol hexaphosphate is the major source of P
(Richardson, 2001; George et al., 2004, 2005a). However,
when grown in most soils these plants have comparable
growth and P nutrition to control plants (George et al., 2004,
2005b). Similarly, overexpression of a bacterial citrate synthase gene in tobacco has been reported to increase citrate
efflux from roots and to increase the availability of P from
calcium phosphate (López-Bucio et al., 2000), but an effect
on plant growth and P acquisition is not always observed
(Delhaize et al., 2001). The expression of a wheat malate
transporter gene (ALMT1) in barley (Hordeum vulgare) has
321
been shown to be effective in increasing P uptake by transgenic plants, but only in severely acidic soil conditions (Delhaize
et al., 2009).
Mutations altering root morphology also have the potential
to enable plants to acquire more P. For example, barley genotypes with long root hairs have higher yields than genotypes
with no root hairs on soils with low P availability (Gahoonia
and Nielsen, 2004; Brown et al., 2012), and genotypes of
bean, maize and brassica with larger root systems have better
growth under P-limiting conditions (Rubio et al., 2003; Liu
et al., 2004; Hammond et al., 2009). The differential expression of a number of transcription factors and genes have
been shown to be critical in greater accumulation of P in
plants (Bari et al., 2006; Chiou et al., 2006). For example, a
T-DNA insertional knockout of a specific arabidopsis gene
(AtSIZ1) caused exaggerated Pi starvation responses, including
increase in root/shoot biomass quotient, cessation of primary
root growth and extensive lateral root development and
increased root hair production, even though intracellular Pi
concentrations in siz1 plants were similar to wild type.
Mutations that improve plant growth through better physiological utilization of P when soil P availability is low can
also be incorporated in breeding programmes to develop
crops for reduced P inputs (Veneklaas et al., 2012). For
example, OsPTF1, a bHLH transcription factor from rice,
whose expression increases in the roots of P-starved plants,
has been shown to enhance tolerance to P starvation (Yi
et al., 2005). Recently, a gene for P-use efficiency in rice
(Pup-1) has been cloned and shown to affect the proliferation
of roots when present (Gamuyao et al., 2012). Thus, we appear
to be on the cusp of being able to deploy a number of postgenomic tools to develop crop germplasm that will allow
improved P acquisition and greater physiological P utilization
(Hammond and White, 2011; Veneklaas et al., 2012).
ROOT - H A I R T R A I T S FO R T H E S E CO N D G R E E N
R E VOL U T I O N
An examination of Table 1 reveals one of the most effective
and least costly of all the P-acquisition mechanisms to be
the production of root hairs and, as such, this trait is a good
candidate for manipulation to improve the sustainability of
agriculture.
Root hair formation, length and longevity have been demonstrated to be regulated by P supply in several crops (e.g. Fohse
and Jungk, 1983; Hoffmann and Jungk, 1995; White et al.,
2005) and also in Arabidopsis thaliana (Bates and Lynch,
1996, 2000). In addition, genetic variation in root-hair length
has been found in many plant species including wheat,
barley, clover, bean, turfgrass and soybean (Caradus, 1979;
Green et al., 1991; Yan et al., 1995; Gahoonia and Nielsen,
1997; Wang et al., 2004). Breeding programmes for white
clover have been able to select for the root-hair length trait
due to its highly heritable nature (Caradus, 1981). Variation
in root-hair length within crop species has been shown to correlate with P acquisition (Gahoonia et al., 1999) and yield
under P-limited conditions (Brown et al., 2012) and experiments using the bald root barley (brb) mutant have provided
a general understanding of the importance of root hairs to P acquisition and crop yield (Gahoonia and Nielsen, 2003).
322
Brown et al. — Root hair ideotypes for future agroecosystems
Root-hair trait responses to P deficiency include alterations
to the length and density of root hairs and the location and
size of the root-hair zone (Foehse and Jungk, 1983; Bates
and Lynch, 1996; Ma et al., 2001a, b). Root hairs tend to be
sparse in P sufficient plants, but increase in length and
density as plants become P deficient (Gahoonia and Nielsen,
1997), with benefits of root hairs for P acquisition reaching a
maximum when P-depletion zones around each root hair
begin to overlap (Ma et al., 2001b). Newly formed root hairs
become sites for expression of genes encoding phosphate
transporters (Mudge et al., 2002) and also release and disperse
root exudates throughout the rhizosphere (Hinsinger, 2001;
Ryan et al., 2001). The structure of root hairs makes them efficient at foraging for P in cracks or pores where roots themselves are unable to penetrate (Misra et al., 1988). Although
the metabolic cost of root hairs might be critical in some situations (Brown et al., 2012), and root hair formation is often correlated with greater metabolic costs associated with organic
acid exudation and P transporters (Lynch and Ho, 2005), the
direct cost of carbon allocation to root hairs is generally considered minimal (Bates and Lynch, 2000).
The size of P-depletion zones around plant roots can be
manipulated by modifications to root-hair length such that an increase in root-hair length allows the depletion zone to expand
around the root providing the plant with access to untapped
sources of P. In addition, root hairs are thought to be critical
in the formation of rhizosheaths (Moreno-Espindola et al.,
2007; Haling et al., 2010 a, b; Brown et al., 2012) which are
physical features of the rhizosphere forming the most intimate
interface between the soil and root. The importance of rhizosheath size to P acquisition is derived from the corresponding
surface area of the root coming into contact with the rhizosphere.
P extracted by a unit length of root. The details of the construction of this model can be found in Supplementary Data. In this
model, the root is represented as a cylinder of radius R0 (cm)
and length of 1 cm. Root hairs are distributed homogeneously
along this cylinder at branching density r (cm21) and form a
radius R1 (cm) around the root (Fig. 1A). We assume root
hairs expand radially in straight lines and, therefore, the
root-hair-length density rl (cm cm23) is determined as a function of the radial distance from the root centreline R: rl(R) ¼ r/
2pR.
The fraction of soil accessed by root hairs is a function of
the root-hair-length density. The greater the root-hair-length
density, the larger the fraction of soil is exploited. The fraction of soil f accessed by root hairs in a unit volume of soil
is a non-decreasing function of root-hair-length density and
tends towards a maximum value of 1. The increase slows
down gradually as roots occupy a larger volume of soil
(Fig. 1B). The relationship between length/density and soil
fraction available to roots has been defined previously as
the principle of proportional resource capture (Dupuy and
Vignes, 2012). In order to understand this principle, it is
useful to consider the region of soil accessed by a portion
of root as a cylinder of radius r. If the fraction of soil accessible to roots is f, then the probability of the new portion of
the root entering a new region of soil is (1 – f )pr 2. The increase of the fraction of soil accessible per unit added root
length/density can therefore be expressed using a differential
equation in which solution f ¼ 1 – exp( – pr 2rl ); explanations of further simplifications to the model can be found
in the Supplementary Data.
Model parameterization and validation
M O D E L L I N G T H E R E L AT I O N S H I P B E T W E E N
CO S T S O F RO OT H A IR P H E NOT Y P E S A ND P
DEPLETION
To test the functionality of root-hair traits, we created a model
to represent how root-hair length, root-hair density along the
root and the longevity of root hairs determine the amount of
A
R1
R0
rb
We used root-hair density values (r ¼ 500 cm21) typical of
those reported in the literature (Tinker and Nye, 2000; Ma
et al., 2001b). Data for root diameter R0 (0.5 mm) and roothair length R1 – R0 (0.7 mm) were derived from experimental
work by Brown et al. (2012; L. K. Brown, T. S. George, G. E.
Barrett, S. McLaren, S. F. Hubbard and P. J. White, unpubl.).
We used values for the phosphate diffusion coefficient D (10 –
B
rl = rb/2pR
1 cm
1
j
rl
F I G . 1. (A) Geometrical representation and parameterization of the root hair distribution on a unit length of root. (B) Representation of the fraction of soil available to roots as a function of root-hair-length density.
Brown et al. — Root hair ideotypes for future agroecosystems
Specific P uptake (µM cm–1, × 10–5)
7
A
6
5
4
3
2
RH density
RH length
RH longevity
1
0
0
0·20
0·5
1·0
1·5
2·0
B
0·15
Cost function
9 cm2 s21) typical of that used in previous work by Ma et al.
(2001a, b). We assumed a root hair longevity T of 5 d. The rate
of P release is determined according to Özacar’s First Order
Kinetic Model for Phosphate, with k ¼ 0.05D[P] mM min21.
D[P] (50 mM) is the difference in concentration between
solid phase P and solution P (Özacar, 2003).
Based on these assumptions, model predictions were compared with the average plant P content per unit root length measured in barley cultivars grown in the glasshouse (Brown et al.,
2012; L. K. Brown, T. S. George, G. E. Barrett, S. McLaren,
S. F. Hubbard and P. J. White, unpubl.). In the experiments of
Brown et al. (2012; L. K. Brown, T. S. George, G. E. Barrett,
S. McLaren, S. F. Hubbard and P. J. White, unpubl.), plants
were grown for 7 d and had, on average, a total root length of
170 cm. The shoot dry weight was 0.04 g. Root dry weight
was not derived, but for the estimation of total plant P content,
we assumed a root dry weight of 0.01 g. The plant P concentration equalled 3 mg P g21 dry matter. Using these values, we
calculated the specific P uptake (total accumulated P per unit
root length) per unit root length of 8.8 1024 mg P cm21 root.
The model underestimates the observed total P content per
unit root length and predicts a total P content per unit root
length in the order of 1025 mM cm21 (Fig. 2). It is likely
that differences between the observed and modelled total
P content per unit root length might be explained by the rate
at which P is replenished in the rhizosphere, due to processes
such as root exudation and the release of phosphatases.
Model predictions show that due to competition with other
root hairs, root-hair density has less effect on P acquisition
than any other root-hair trait (Fig. 2). Unless root-hair length
is increased drastically at the same time, less is to be gained
by increased root-hair density. Root-hair length is the trait
that has the largest effect on P uptake (Fig. 2). The cost of increasing root-hair traits, however, might be prohibitive, particularly due to the physical constraints to growth and
maintenance of long root-hair cells. Longevity has less
impact on P uptake than root-hair length (Fig. 2), but the
benefit is in the same order of magnitude. It is likely also
that longevity has low physiological cost and holds more
promise to improve P acquisition than other traits. However,
this is only true in the case where the limiting factor is the
P-replenishment rate. In the case where the limiting factor is
total soil P, longevity will have a similar effect on P acquisition as root-hair density.
Costs for root-hair length, density and longevity used exponential empirical functions with constant growth rates, b1, b2
and b3, and varying amplitudes a1, a2 and a3 for root-hair
density, length and longevity, respectively. In order to infer
the value of the parameters of the cost functions, we made the
hypothesis that current genotypes are close to an optimal P
uptake. Results show that cost functions follow the same order
as the efficiency of each of the root traits: root-hair length
(a2 ¼ 0.13) has the highest improvement cost, root-hair longevity has an intermediate cost (a3 ¼ 0.096) and root-hair density
has the lowest improvement cost (a1 ¼ 0.0018) (Fig. 3). To summarize, root-hair density has a low cost but is quite inefficient at
generating increased P uptake, and root-hair length is efficient at
improving P uptake but the associated costs are the highest.
Optimal root-hair traits for low P soils can be derived from
this analysis. For example, if P availability is reduced by
323
0·10
0·05
0
0
RH density
RH length
RH longevity
0·5
1·0
1·5
2·0
Fold change with respect to WT
F I G . 2. Specific P uptake and calculated cost associated with root-hair (RH)
traits. (A) Influence of root-hair density, root-hair length and root-hair longevity on specific P uptake. The x-axis indicates the fraction of the change in
density, length and longevity with respect to wild type (WT). The y-axis indicates the corresponding changes in specific P uptake. (B) Estimated cost function for root-hair density, root-hair length and root-hair longevity. The x-axis
indicates the fraction of the change in density, length and longevity with
respect to wild type (WT). The y-axis is the cost of building these traits.
15 %, the new optimal root-hair traits will require 3.5 % increase in root-hair density, 6.9 % increase in root-hair
length, and root-hair longevity would have to be increased
by 6.2 %. In this new configuration, specific P uptake would
be reduced by 0.7 %. This analysis provides insights into the
type of modifications that would allow crops to maintain
yield under reduced P availability. Further research should
now concentrate on the quantification of the physiological
costs associated with root-hair traits. These cost functions
will be critical to predict accurately the performance of ideotypes in field conditions.
324
Brown et al. — Root hair ideotypes for future agroecosystems
120
RO OT H AI R I DE OT Y P E S FO R I NC R E A S E D P
ACQU IS ITI ON IN B AR LEY
5
Root architectural ideotype: increasing the surface area of root
hairs in P-replete soil
0
100
Log cost
10
80
–5
60
2
40
20
–10
4
0
0·10
6 Longevity
–15
0·08
0·06
Root hair length
0·04
8
F I G . 3. Shape of the cost function on a subset of the trait space. The z-axis
represents total cost and colourmap indicates variations from optimal P acquisition. The x-axis indicates root-hair length, the y-axis indicates root-hair longevity and the z-axis indicates the cost of making these traits. The vertical line
indicates the optimal set of root-hair traits under a 15 % reduction in P availability. The new optimal root-hair traits will require a 3.5 % increase in roothair density, a 6.9 % increase in root-hair length, and root-hair longevity would
have to be increased by 6.2 %. In this new configuration, specific P uptake
would be reduced by 0.7 %.
CO NCE P TUA L MO DE L OF BA RLEY RO OT -H AI R
F U N C T I O N I N P - L I M I T E D E N V I RON M E N T S
By combining insights from studies in the literature, the
model described above and our recently published experiments we have produced a conceptual model of barley roothair function in P-limited environments which identifies
targets for future breeding programmes for improved P acquisition (Fig. 4). Our recent results have established that the
presence of root hairs is implicit to the sustainable yield of
barley in P-limiting conditions; however, root-hair length is
not important in maintaining yield under these conditions
(Brown et al., 2012). Further investigations into the possible
compensatory role of AM fungi in P acquisition indicated
that significant AM colonization is only found in barley
plants lacking root hairs, and that AM associations did not
provide an effective compensatory mechanism for P acquisition in the absence of root hairs (L. K. Brown, T. S. George,
G. E. Barrett, S. McLaren, S. F. Hubbard and P. J. White,
unpubl.). Therefore, genotypes with root hairs of an
optimum length and density, producing a contiguous depletion zone, with no mycorrhizal infection appear to perform
best (Figs 2 and 4). It should be noted that due to the
large genotypic variation in traits such as root-hair length
among different barley cultivars (Gahoonia and Nielsen,
2004), this conceptual model might not hold true for all cultivars, and this is important to bear in mind when breeding
for optimum P acquisition, i.e. genotypes with shorter root
hairs may benefit from increased root-hair length. Our
results and modelling suggest that the ideal root-hair zone
would be comprised of contiguous root hair depletion
zones with variable longevity which would allow soil exploration to be maximized but would not waste valuable energy
as a result of the competition between root hairs.
Increasing the length and/or density of root hairs increases the
potential of a plant to acquire P. One architectural ideotype for
improving P acquisition would include an increase in the
numbers of root hairs in surface soils where the majority of
P is found. This could be achieved in two ways: (1) by increasing the density of root hairs within existing root-hair zones or
(2) by modifying root architecture to increase the number of
root-hair zones by producing more roots.
There is an optimum root-hair length and root-hair density
for the most efficient P acquisition which is determined
when P-depletion zones around each root hair begin to
overlap (see Fig. 4; Ma et al., 2001a). This concept of competition between root hairs within the root-hair zone is an important consideration when looking at potential ways of increasing
the number of root hairs.
Increasing the number of roots and root branches will increase the number of root-hair zones. The potential to couple
this with the ability of the plant to respond to P deficiency
by proliferating their roots in the P-rich surface layers of soil
(Lynch and Brown, 2001) and/or nutrient-rich patches
(Hodge, 2004) will have the effect of concentrating more roothair zones in the areas where most P is available. It should be
noted, however, that the metabolic costs of soil exploration by
root systems are substantial and can exceed 50 % of daily
photosynthesis (Lambers et al., 2002).
Root anatomical ideotype: reducing the cost of root hairs
Another proposed component of the root-hair ideotype is
based on the idea that P acquisition by root hairs can be
enhanced by increasing the longevity of the individual root
hairs. The typical active life of a functional root hair for nutrient acquisition is only a few days (McElgunn and Harrison,
1969). In contrast the cell walls of root hairs often remain
for many days, long after the root hair cells have ceased to
function (Clarkson, 1996). Because of the short life of individual root hairs, the root-hair zone ‘moves’ through the soil by
continuously changing its location following the growth of
the root apex, and the period of time for contact between
root hairs and soil at a specific location is determined by the
lifetime of the root hair. The data of Claassen et al. (1981) suggests that the soil surrounding root-hair zones becomes
depleted of available P within a few days and an increase in
the longevity of root hairs to greater than a few days would,
therefore, not increase P acquisition (Jungk, 2001). However,
the time taken to exhaust the soil of available P is likely to
vary greatly depending on soil type, being much shorter in extremely P-deficient soils than in the less-deficient soils which
are likely to be typical of future low-input agricultural systems.
However, it is not known whether all genotypes have root hairs
whose longevity is sufficient to take advantage of the available
P and we could hypothesize that increased plant available P
could be accessed by increasing the functional life of a root
hair, thereby keeping high affinity P transporters operational
for longer. While the P concentration of the soil decreases
Brown et al. — Root hair ideotypes for future agroecosystems
325
Intensive
Modification
1
Extensive
1b
1a
Architectural
Hordeum vulgare
‘Optic’
Longer / more root hairs
Overlapping
depletion
zones
More root hair zones
in surface
Increased root hair
surface area
2a
2b
2
Anatomical
Breeding
pressure /
Natural
selection
No change
Contiguous
depletion
zones
Root hair zones on lowcost root
Long-lived root hair zones
3a
3a
3
Biochemical
No root hairs / AM fungi
AM fungi
depletion
zones
Root hair zones delivering
exudates
Root hair zones recruiting
beneficial microbes
F I G . 4. Conceptual model of root hair contribution to P acquisition: a synthesis of experimental results, conclusions taken from literature and hypotheses suggesting targets for future breeding programmes for improved P acquisition in barley. Modifications to root hairs in barley (Hordeum vulgare ‘Optic’) resulting
from breeding pressure or natural selection are highlighted in modifications 1–3. Root-hair zones are identified by straight graduating light brown lines.
Modification 1 represents an increase in root-hair numbers and length and the inset demonstrates the resulting overlap of P-depletion zones which are
defined by red dotted lines. Modification 2 represents the optimum status, which in the case of the Optic cultivar, means no change. Here the inset demonstrates
a zone of contiguous root-hair zones with the extent of the P-depletion zone defined by the red dotted lines. Modification 3 represents a scenario where no root
hairs are present and the roots are colonized by AM fungi which produce a P-depletion zone identified by the pink highlighted area surrounding the roots in the
inset. The associated yield for each modification is represented by the green barley heads, the greater the number the greater the yield. Potential target traits or
ideotypes for improving P acquisition are divided into the three categories. (1) Architectural – (a) intensive: increasing the total root-hair surface area (more red
root-hair zones on more roots); (b) extensive: increasing the number of red root-hair zones in the surface area of soil where the greatest amount of P is typically
found. (2) Anatomical – (a) intensive: longer-living root hairs represented by green root-hair zones; (b) extensive: red root-hair zones on low-cost green roots. (3)
Biochemical – (a) intensive: root-hair zones delivering exudates represented by yellow dots; (b) extensive: root-hair zones recruiting beneficial microbes represented by blue circles.
quickly around newly formed root hairs, this is slowly replenished through the processes of diffusion and mineralization. As
such, root hairs which remain functional for longer might be
able to acquire more P. Increasing the longevity might also increase the amount of P-liberating compounds that can be
exuded by the root hair, thereby having greater potential for
liberating more plant-available P.
The allocation of root-hair zones to less metabolically
demanding root classes is another way of achieving more roothair zones at a minimum cost. Miller et al. (2003) have shown
that adventitious roots acquire P at reduced metabolic cost
compared with basal or tap roots and the relative biomass of
adventitious roots increases under P-deficit conditions.
Targeting root-hair zones to roots with aerenchyma could
greatly improve the efficiency with which roots take up
P. Indeed, there may be potential for the ‘saving’ associated
with this root formation to ‘pay’ for the additional cost of
more root-hair zones. In addition, increased root turnover
could potentially improve P acquisition by increasing soil exploration and replacing older roots with younger ones which
are more active in P uptake (Steingrobe et al., 2001). The roothair zones associated with the new roots will enhance P acquisition while the senescence of the older roots will allow the
remobilization of resources, thereby, reducing the metabolic
cost of maintenance respiration.
Biochemical modifications to rhizosphere ideotype: extracting
more from root-hair zones
The production and secretion of phosphatases and the exudation of organic anions by roots, particularly in the root-hair
zone where the potential for P uptake is greatest, could
326
Brown et al. — Root hair ideotypes for future agroecosystems
increase P acquisition by plants. Significant genotypic variation in the secretion of organic acids and phosphatases has
been observed both between and within plant species
(Asmar, 1997; Wouterlood et al., 2004; Richardson et al.,
2005; George et al., 2008).
The ultimate ideotype to target with regards root hairs and
exudation is similar to that of cluster roots formed by a
number of species including Lupinus albus (Neumann et al.,
1999). An ideotype which targets root-hair zones with an
enhanced ability to exude organic anions, followed temporally
by phosphatases, is likely to maximize the potential to liberate
plant-available P in the zone surrounding root hairs where it
can be readily taken up (George et al., 2005a). The order in
which these compounds are released could be crucial in increasing plant-available P whereby the release of organic
acids would prime soil conditions with soluble Po prior to
increased phosphatase activity which would enhance mineralization. With exudates representing 5 – 25 % of photosynthate
production in species producing cluster roots (Dinkelaker
et al., 1995), the targeting of enhanced exudation in the roothair zones, where the high affinity phosphate transporters are
found, could help reduce the substantial metabolic investment
involved in exudate production.
Root-hair zones might also deliver compounds to select specific microbial communities with a greater ability to increase P
availability to plants. This could be through selection of microorganisms which produce phytohormones to enhance root
growth, those which produce P-active exudates and those
which turnover rapidly releasing P for plant consumption. In
order to screen for this trait the functionality of individual microbial species would need to be understood and the identity of
appropriate compounds secreted by plants established.
The lack of a role for AM fungi
None of the ideotypes suggested in this conceptual model
for barley include AM fungi. While associations with AM
fungi have been demonstrated to improve P nutrition of
many plant species (Smith et al., 2003), the conclusions of
Brown et al. (L. K. Brown, T. S. George, G. E. Barrett, S.
McLaren, S. F. Hubbard and P. J. White, unpubl.) suggest
that AM associations do not play a significant role in P acquisition in barley and might even have a detrimental effect.
Hence, Brown et al. (L. K. Brown, T. S. George, G. E.
Barrett, S. McLaren, S. F. Hubbard and P. J. White, unpubl.)
suggest that barley breeding programmes should focus on
maintaining or improving other root traits such as increased
root-hair length, density and longevity or greater exudation
of P-liberating compounds.
I M P L I CAT IO NS FOR F U T U R E BR E E DI NG
P RO G R A M M E S
Improved understanding of root-hair traits involved in P acquisition will help new cultivar breeding programmes. Screening
of populations for phenotypes associated with root traits is a
useful, though time-consuming, approach (Lynch, 2007).
Such breeding programmes should exploit the large genotypic
variation in root-hair traits associated with enhanced P acquisition. Importantly, it has been observed that many traits
present in traditional landraces and older cultivars may have
been bred out of modern-day genotypes which are adapted
to high-input, intensive agricultural systems (Bingham et al.,
2012). It is traits like these that may now be of value in the
current context of finite resources and the need to increase
the productivity of poorer soils through the reintroduction of
genes regulating such adaptive traits. The impact of the environment on genotype should also be taken into consideration
and screens for new crops adapted to problem or marginal
soils should be carried out under low-input conditions in the
presence of biotic and abiotic stresses. Where soils are less
problematic it is possible that modifications to only a single
root-hair trait may be sufficient to enhance access to
P. When considering which traits to target for improved P acquisition it is important to keep any costs to the plant to a
minimum. The benefit of modifying root-hair traits for
improved P acquisition depends on the relative metabolic
and ecological costs associated with the trait compared with
the benefits of the improved P acquisition. Root costs have
been found to be particularly important in plants under P
stress (Lynch and Ho, 2005).
In addition to the need to balance the potential costs and
benefits to the plant of the various ideotypes, it is clear that
a combination of these traits would provide optimum P acquisition. Under severe P deficiency the combined benefits of
increased number and longevity of root hairs are likely to increase P acquisition. This can be complimented by increased
exudation of P-liberating compounds. Breeding programmes
which involve the integration of P absorption, solubilization
and mineralization traits are likely to produce the greatest benefits to P acquisition. Furthermore, superior fitness will be
achieved by genotypes that can acquire limited soil resources
at reduced metabolic cost, as they can allocate more metabolic
resources to defence, growth and reproduction.
Breeding programmes should also consider the implications
of phenotypic plasticity (Zhu et al., 2010) that helps to maximize P acquisition without wasting valuable carbon resources.
Plasticity in the expression of selected root traits to improve P
acquisition is preferable to constitutively expressed traits with
the consequential metabolic costs of these modifications only
being incurred in P-limiting conditions.
While the conceptual model presented here has focused on
one species (barley) the principles and concepts behind its creation could be easily adapted to other species, given an understanding of the specific adaptive traits and mechanisms that
they employ, e.g. the optimum root-hair-length density, the
ability of the plant to liberate plant-available P through modifications to rhizosphere biochemistry and its relationships with
other microorganisms such as AM fungi. The use of such a
model to improve our understanding of the relative importance
of the various root-hair traits involved in improving P acquisition for different species could allow breeders to tailor their
programmes to produce optimum genotypes for each crop
species.
Ideotypes with root-hair traits or a combination of root-hair
traits, e.g. increased numbers of root hairs/root-hair zones,
increased longevity of root hairs and increased exudation of
P-liberating compounds have the potential to improve the P efficiency of crop plants. It is traits such as these that should be
targeted through breeding programmes to increase crop
Brown et al. — Root hair ideotypes for future agroecosystems
production while reducing the environmental impact and improving the long-term sustainability of agriculture. The fact
that the genetic control of some of these traits is already
known, as highlighted previously, means that their deployment
in current germplasm could be relatively rapid. Developments
which improve the efficiencies by which humans utilize finite
resources such as phosphate have the potential to make a contribution on a global scale in a future of population growth and
environmental change.
S U P P L E M E N TARY D ATA
Supplementary data are available online at www.aob.oxfordjournals.org and consist of details of the mathematical model
representing how root-hair length, root-hair density along the
root and the longevity of root hairs determine the amount of
P extracted by a unit length of root.
L I T E R AT U R E C I T E D
Asmar F. 1997. Variation in activity of root extracellular phytase between genotypes of barley. Plant and Soil 195: 61– 64.
Bar-Yosef B. 1991. Root excretions and their environmental effects: influence
on availability of phosphorus. In: Waisel Y, Eshel A, Kafkafi U. eds.
Plant roots: the hidden half. New York, NY: Marcel Dekker, 529– 557.
Barber SA. 1995. Soil nutrient bioavailability: a mechanistic approach, 2nd
edn. New York, NY: Wiley.
Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C. 2005. Microbial cooperation in the rhizosphere. Journal of Experimental Botany 56:
1761–1778.
Bari R, Pant BD, Stitt M, Scheible WR. 2006. Pho2, microRNA399, and
PHR1 define a phosphate-signaling pathway in plants. Plant Physiology
141: 988–999.
Bates TR, Lynch JP. 1996. Stimulation of root hair elongation in Arabidopsis
thaliana by low phosphorus availability. Plant, Cell & Environment 19:
529– 538.
Bates TR, Lynch JP. 2000. The efficiency of Arabidopsis thaliana
(Brassicaceae) root hairs in phosphorus acquisition. American Journal
of Botany 87: 964 –970.
Bingham IJ, Karley AJ, White PJ, Thomas WTB, Russell JR. 2012.
Analysis of improvements in nitrogen use efficiency associated with 75
years of barley breeding. European Journal of Agronomy 42: 49– 58.
Brown LK, George TS, Thompson JA, et al. 2012. What are the implications
of variation in root hair length on tolerence to phosphorus deficiency in
combination with water stress in barley (Hordeum vulgare L.)? Annals
of Botany 110: 319–328.
Caradus JR. 1979. Selection for root hair length in white clover (Trifolium
repens L.). Euphytica 28: 489– 494.
Caradus JR. 1981. Effect of root hair length on white clover growth over a
range of soil phosphorus levels. New Zealand Journal of Agricultural
Research 24: 359– 364.
Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CI. 2006. Regulation of
phosphate homeostasis by microRNA in Arabidopsis. The Plant Cell 18:
412– 421.
Claassen N, Hendriks L, Jungk A. 1981. Determination of the nutrient distribution in the soil–root interface by autoradiograpphy. Zeitschrift fur
Pflanzenernahrung und Bodenkunde 144: 306–316.
Clark RB, Zeto SK. 2000. Mineral acquisition by arbuscular mycorrhizal
plants. Journal of Plant Nutrition 23: 867– 902.
Clarkson D T. 1996. Root structure and sites of ion uptake. In: Waisel Y,
Eshel A, Kafkafi U. eds. Plant roots: the hidden half. New York, NY:
Marcel Dekker, 417– 453.
Cordell D, Drangert J-O, White S. 2009. The story of phosphorus: global
food security and food for thought. Global Environmental Change 19:
292– 305.
Dawson CJ, Hilton J. 2011. Fertiliser availability in a resource-limited world:
production and recycling of nitrogen and phosphorus. Food Policy 36:
S14–S22.
327
Delhaize E, Hebb DM, Ryan PR. 2001. Expression of a Pseudomonas aeruginosa citrate synthase gene is not associated with either enhanced citrate
accumulation or efflux. Plant Physiology 125: 2059– 2067.
Delhaize E, Taylor P, Hocking PJ, Simpson RJ, Ryan PR, Richardson AE.
2009. Transgenic barley (Hordeum vulgare L.) expressing the wheat aluminium resistance gene (TaALMT1) shows enhanced phosphorus nutrition and grain production when grown on an acid soil. Plant
Biotechnology Journal 7: 391– 400.
Devau N, Le Cadre E, Hinsinger P, Gérard F. 2010. A mechanistic model
for understanding root-induced chemical changes controlling phosphorus
availability and bioavailability. Annals of Botany 105: 1183– 1197.
Devau N, Hinsinger P, Le Cadre E, Gérard F. 2011. Root-induced processes
controlling phosphate availability in soils with contrasted P-fertilized
treatments. Plant and Soil 348: 203– 218.
Dinkelaker B, Romheld V, Marschner H. 1989. Citric-acid excretion and
precipitation of calcium citrate in the rhizosphere of white lupin
(Lupinus-albus L.) Plant, Cell & Environment 12: 285 –292.
Dinkelaker B, Hengeler C, Marschner H. 1995. Distribution and function of
proteoid rests and other root clusters. Botanica Acta 108: 183 –200.
Douds DD, Johnson CR, Koch KE. 1988. Carbon cost of the fungal symbiont
relative to net leaf-P accumulation in a split-root VA mycorrhizal symbiosis. Plant Physiology 86: 491– 496.
Dupuy L, Vignes M. 2012. An algorithm for the simulation of the growth of
root systems on deformable domains. Journal of Theoretical Biology
310:164–174.
Eissenstat DM. 1992. Costs and benefits of constructing roots of small diameter. Journal of Plant Nutrition 15: 763 –782.
Eissenstat DM, Graham JH, Syvertsen JP, Drouillard DL. 1993. Carbon
economy of sour orange in relation to mycorrhizal colonization and phosphorus status. Annals of Botany 71: 1 –10.
Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL. 2000. Building roots in
a changing environment: implications for root longevity. New Phytologist
147: 33– 42.
Fan MS, Zhu JM, Richards C, Brown KM, Lynch JP. 2003. Physiological
roles for aerenchyma in phosphorus-stressed roots. Functional Plant
Biology 30: 493–506.
Feng G, Song YC, Li XL, Christie P. 2003. Contribution of arbuscular
mycorrhizal fungi to utilization of organic sources of phosphorus by
red clover in a calcareous soil. Applied Soil Ecology 22: 139–148.
Fitter AH. 1985. Functional significance of root morphology and root system
architecture. In: Fitter AH. ed. Ecological interactions in soil: plants,
microbes and animals (Special Publication No. 4 of the British
Ecological Society). Oxford: Blackwell Science, 87– 106.
Foehse D, Jungk A. 1983. Influence of phosphate and nitrate supply on root
hair formation of rape, spinach and tomato plants. Plant and Soil 74:
359–368.
Forde B, Lorenzo H. 2001. The nutritional control of root development. Plant
and Soil 232: 51– 68.
Gahoonia TS, Care D, Nielsen NE. 1997. Root hairs and phosphorus acquisition of wheat and barley cultivars. Plant and Soil 191: 181– 188.
Gahoonia TS, Nielsen NE. 1999. Root hairs of phosphorus-efficient cereal
cultivars. In: Lynch JP, Deikman J. eds. Phosphorus in plant biology:
regulatory roles in molecular, cellular, organismic, and ecosystem processes (Proceedings 12th Annual Penn State Symposium in Plant
Physiology, 19). ASPP, 319–321.
Gahoonia TS, Nielsen NE. 2003. Phosphorus (P) uptake and growth of a root
hairless barley mutant (bald root barley, brb) and wild type in low- and
high-P soils. Plant, Cell & Environment 26: 1759–1766.
Gahoonia TS, Nielsen NE. 2004. Barley genotypes with long root hairs
sustain high grain yields in low-P field. Plant and Soil 262: 55–62.
Gamuyao R, Chin JH, Pariasca-Tanaka J, et al. 2012. The protein kinase
Pstol1 from traditional rice confers tolerance of phosphorus deficiency.
Nature 488: 535–539.
Gardner WK, Boundy KA. 1983. The acquisition of phosphorus by Lupinus
albus L. 4. The effect of interplanting wheat and white lupin on the
growth and mineral-composition of the 2 species. Plant and Soil 70:
391–402.
Ge ZY, Rubio G, Lynch JP. 2000. The importance of root gravitropism for
inter-root competition and phosphorus acquisition efficiency: results
from a geometric simulation model. Plant and Soil 218: 159– 171.
George TS, Gregory PJ, Wood M, Read D, Buresh RJ. 2002. Phosphatase
activity and organic acids in the rhizosphere of potential agroforestry
species and maize. Soil Biology & Biochemistry 34: 1487– 1494.
328
Brown et al. — Root hair ideotypes for future agroecosystems
George TS, Richardson AE, Hadobas PA, Simpson RJ. 2004.
Characterization of transgenic Trifolium subterraneum L. which expresses
phyA and releases extracellular phytase: growth and P nutrition in laboratory media and soil. Plant, Cell & Environment 27: 1351–1361.
George TS, Richardson AE, Smith JB, Hadobas PA, Simpson RJ. 2005a.
Limitations to the potential of transgenic Trifolium subterraneum
L. plants that exude phytase when grown in soils with a range of
organic P content. Plant and Soil 278: 263–274.
George TS, Simpson RJ, Hadobas PA, Richardson AE. 2005b. Expression
of a fungal phytase gen in Nicotiana tabacum improves phosphorus nutrition in plants grown in amended soil. Plant Biotechnology Journal 3:
129–140.
George TS, Gregory PJ, Hocking P, Richardson AE. 2008. Variation in
root-associated phosphatase activities in wheat contributes to the utilization of organic P substrates in vitro, but does not explain differences in the
P-nutrition of plants when grown in soils. Environmental and
Experimental Botany 64: 239– 249.
Green RL, Beard JB, Oprisko MJ. 1991. Root hairs and root lengths in nine
warm-season turftgrass genotypes. Journal of the American Society for
Horticultural Science 75: 457–461.
Gregory PJ, George TS. 2011. Feeding the nine billion: the challenge to sustainable crop production. Jounal of Experimental Botany 62: 5233– 5239.
Gilbert N. 2009. The disappearing nutrient. Nature 461: 716– 718.
Haling RE, Richardson AE, Culvenor RA, Lambers H, Simpson RJ.
2010a. Root morphology, root-hair development and rhizosheath formation on perennial grass seedlings is influenced by soil acidity. Plant
and Soil 335: 457– 468.
Haling RE, Simpson RJ, Delhaize E, Hocking PJ, Richardson AE. 2010b.
Effect of lime on root growth, morphology and the rhizosheath of cereal
seedlings growing in an acid soil. Plant and Soil 327: 199– 212.
Hammond JP, White PJ. 2011. Sugar signalling in root responses to low
phosphorus availability. Plant Physiology 156: 1033–1040.
Hammond JP, Bennett MJ, Bowen HC, et al. 2003. Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential
for developing smart plants. Plant Physiology 132: 578–596.
Hammond JP, Broadley MR, White PJ. 2004. Genetic responses to phosphorus deficiency. Annals of Botany 94: 323– 332.
Hammond JP, Broadley MR, White PJ, et al. 2009. Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architectural traits. Journal of Experimental Botany 60: 1953–1968.
Harris D, Paul E. 1997. Carbon requirements of vesicular-arbuscular mycorrhizae. In: Safir GR. ed. Ecophysiology of VA mycorrhizae. Boca Raton,
FL: CRC, 93–105.
Helal HM, Dressler A. 1989. Mobilization and turnover of soil phosphorus in
the rhizosphere. Zeitschrift für Pflanzenernahrung und Bodenkunde 152:
175–180.
Hermans C, Hammond JP, White PJ, Verbruggen N. 2006. How do plants
respond to nutrient shortage by biomass allocation? Trends in Plant
Science 11: 610– 617.
Hill JO, Simpson RJ, Moore AD, Chapman DF. 2006. Morphology and response of roots of pasture species to phosphorus and nitrogen nutrition.
Plant and Soil 286: 7 –19.
Hinsinger P. 2001. Bioavailability of soil inorganic P in the rhizosphere as
affected by root-induced chemical changes: a review. Plant and Soil
237: 173– 195.
Hinsinger P, Bengough AG, Vetterlein D, Young IM. 2009. Rhizosphere:
biophysics, biogeochemistry and ecological relevance. Plant and Soil
321: 117– 152.
Ho MD, McCannon BC, Lynch JP. 2004. Optimization modeling of plant
root architecture for water and phosphorus acquisition. Journal of
Theoretical Biology 226: 331 –340.
Hodge A. 2004. The plastic plant: root responses to heterogeneous supplies of
nutrients. New Phytologist 162: 9 –24.
Hoffmann C, Jungk A. 1995. Growth and phosphorus supply of sugar beet as
affected by soil compaction and water tension. Plant and Soil 176:
15– 25.
Hood ME, Shew HD. 1997. Initial cellular interactions between Thielaviopsis
basicola and tobacco root hairs. Phytopathology 87: 228– 235.
Jakobsen I, Rosendahl L. 1990. Carbon flow into soil and external hyphae
from roots of mycorrhizal cucumber plants. New Phytologist 115: 77– 83.
Jakobsen I, Leggett ME, Richardson AE. 2005. Rhizoshpere microorganisms and plant phosphorus uptake. In Sims JT, Sharpley AN. eds.
Phosphorus, agriculture and the environment. Madison, WI: American
Society for Agronomy, 437–494.
Johnson JF, Allan DL, Vance CP, Weiblen G. 1996a. Root carbon dioxide
fixation by phosphorus-deficient Lupinus albus: contribution to organic
acid exudation by proteoid roots. Plant Physiology 112: 19–30.
Johnson JF, Vance CP, Allan DL. 1996b. Phosphorus deficiency in Lupinus
albus: altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiology 112: 31– 41.
Jones DL. 1998. Organic acids in the rhizosphere: a critical review. Plant and
Soil 205: 25– 44.
Jones DL, Darrah PR. 1994. Role of root derived organic acids in the mobilization of nutrients in the rhizosphere. Plant and Soil 166: 247–257.
Jones DL, Dennis PG, Owen AG, van Hees PAW. 2003. Organic acid behaviour in soils: misconceptions and knowledge gaps. Plant and Soil 248:
31–41.
Jungk A. 2001. Root hairs and the acquisition of plant nutrients from soil. Journal
of Plant Nutrition and Soil Science – Zeitschrift fur Pflanzenernahrung
und Bodenkunde 164: 121–129.
Keerthisinghe G, Hocking PJ, Ryan PR, Delhaize E. 1998. Effect of phosphorus supply on the formation and function of proteoid roots of white
lupin (Lupinus albus L.). Plant, Cell & Environment 21: 467–478.
Kirk GJD, Santos EE, Findenegg GR. 1999. Phosphate solubilization by
organic anion excretion from rice (Oryza sativa L.) growing in aerobic
soil. Plant and Soil 211: 11–18.
Koch KE, Johnson CR. 1984. Photosynthate partitioning in split root citrus
seedlings with mycorrhizal and non-mycorrhizal root systems. Plant
Physiology 75: 26– 30.
Koide RT, Goff MD, Dickie IA. 2000. Component growth efficiencies of
mycorrhizal and nonmycorrhizal plants. New Phytologist 148: 163– 168.
Lambers H, Aitken O, Millenaar FF. 2002. Respiratory patterns in roots in
relation to their functioning. In: Waisel Y, Eshel A, Kafkafi U. eds. Plant
roots: the hidden half. New York, NY: Marcel Dekker, 521–522.
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ. 2006. Root
structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Annals of Botany 98:
693– 713.
Lamont BB. 2003. Structure, ecology and physiology of root clusters: a
review. Plant and Soil 248: 1 –19.
Li D, Zhu H, Liu K, et al. 2002. Purple acid phosphatase of Arabidopsis thaliana: comparative analysis and differential regulation by phosphate deprivation. Journal of Biological Chemistry 277: 27772–27781.
Li L, Tang C, Rengel Z, Zhang F. 2003. Chickpea facilitates phosphorus
uptake by intercropped wheat from an organic phosphorus source. Plant
and Soil 248, 297– 303.
Liu Y, Mi G, Chen F, Zhang J, Zhang F. 2004. Rhizosphere effect and root
growth of two maize (Zea mays L.) genotypes with contrasting P efficiency at low P availability. Plant Science 167: 217– 223.
Lopez-Bucio J, de la Vega OM, Guevara-Garcı́a A, Herrera-Estrella L.
2000. Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nature Biotechnology 18, 450–453.
Lu Y, Wassmann R, Neue HU, Huang C. 1999. Impact of phosphorus supply
on root exudation, aerenchyma formation and methane emission of rice
plants. Biogeochemistry 47: 203–218.
Lynch JP. 2007. Roots of the second green revolution. Australian Journal of
Botany 55: 493–512.
Lynch JP. 2011. Root phenes for enhanced soil exploration and phoshorus
acquisition: tools for future crops. Plant Physiology 156: 1041–1049.
Lynch JP, Beebe SE. 1995. Adaptation of beans (Phaseolus vulgarus L.) to
low phosphorus availability. Hortscience 30: 1165–1171.
Lynch JP, Brown KM. 1998. Root architecture and phosphorus acquisition
efficiency in common bean. In: Lynch J, Deikman J. eds. Phosphorus
in plant biology: regulatory roles in molecular, cellular, organismic
and ecosystem processess. Rockville, MD: ASPP, 148–154.
Lynch JP, Brown KM. 2001. Topsoil foraging: an architectural adaptation of
plants to low phosphorus availability. Plant and Soil 237: 225 –237.
Lynch JP, Ho MD. 2005. Rhizoeconomics: carbon costs of phosphorus acquisition. Plant and Soil 269: 45– 56.
McElgunn JD, Harrison CM. 1969. Formation elongation and logevity of
barley root hairs. Agronomy Journal 61: 79– 81.
McLaughlin MJ, Alston AM, Martin JK. 1988. Phosphorus cycling in
wheat-pasture rotations. II. The role of the microbial biomass in phosphorus cycling. Australian Journal of Soil Research 26: 333– 342.
Brown et al. — Root hair ideotypes for future agroecosystems
Ma Z, Bielenberg DG, Brown KM, Lynch JP. 2001a. Regulation of root hair
density by phosphorus availability in Arabidopsis thaliana. Plant, Cell &
Environment 24: 459–467.
Ma Z, Walk TC, Marcus A, Lynch JP. 2001b. Morphological synergism in
root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: a modeling approach. Plant and Soil 236:
221– 235.
Macklon AES, Grayston SJ, Shand CA, Sim A, Sellars S, Ord BG. 1997.
Uptake and transport of phosphorus by Agrostis capillaris seedlings from
rapidly hydrolysed organic sources extracted from 32P-labelled bacterial
cultures. Plant and Soil 190: 163– 167.
Marschner H, Romheld V. 1996. Root-induced changes in the availability of
micronutrients in the rhizosphere. In: Waisel Y, Eshel A, Kafkafi U. eds.
Plant roots: the hidden half. New York, NY: Marcel Dekker, 521– 552.
Marschner P. 2008. The role of rhizosphere microorganisms in relation to P
uptake by plants. In: White PJ, Hammond JP. eds. The ecophysiology of
plant– phosphorus interactions. Dordrecht: Springer, 1–7.
Mikkelsen RL. 2000. Beneficial use of swine by-products: opportunities for
the future. In: Powers JF, Dick WA. eds. Land application of agricultural,
industrial, and municipal by-products (SSSA Book Series No. 6).
Madison, WI: SSSA, 451–480.
Miller CR, Ochoa I, Nielsen KL, Beck D, Lynch JP. 2003. Genetic variation
for adventitious rooting in response to low phosphorus availability: potential utility for phosphorus acquisition from stratified soils. Functional
Plant Biology 30: 973– 985.
Misra RK, Alston AM, Dexter AR. 1988. Role of root hairs in phosphorus
depletion from a macrostructured soil. Plant and Soil 107: 11– 18.
Morcuende R, Bari R, Gibon Y, et al. 2007. Genome-wide reprogramming of
metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant, Cell & Environment 30: 85–112.
Moreno-Espindola IP, Rivera-Becerril F, Ferrara-Guerrero MD, De
Leon-Gonzalez F. 2007. Role of root-hairs and hyphae in adhesion of
sand particles. Soil Biology & Biochemistry 39: 2520–2526.
Morgan JAW, Bending GD, White PJ. 2005. Biological costs and benefits to
plant– microbe interactions in the rhizosphere. Journal of Experimental
Botany 56: 1729–1739.
Mudge SR, Rae AL, Diatloff E, Smith FW. 2002. Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. The Plant Journal 31: 341–353.
Neumann G, Martinoia E. 2002. Cluster roots: an underground adaptation for
survival in extreme environments. Trends in Plant Science 7: 162–167.
Neumann G, Massonneau A, Martinoia A, Römheld V. 1999. Physiological
adaptations to phosphorus deficiency during proteiod root development in
white lupin. Planta 208: 373– 382.
Nguyen C. 2003. Rhizodeposition of organic C by plants: mechanisms and
controls. Agronomie 23: 375–396.
Nielsen KL, Bouma TJ, Lynch JP, Eissenstat DM. 1998. Effects of phosphorus availability and vesicular-arbuscular mycorrhizas on the carbon
budget of common bean (Phaseolus vulgaris). New Phytologist 139:
647– 656.
Nielsen KL, Eshel A, Lynch JP. 2001. The effect of phosphorus availability
on the carbon economy of contrasting common bean (Phaseolus vulgaris
L.) genotypes. Journal of Experimental Botany 52: 329– 339.
Oehl F, Oberson A, Sinaj S, Frossard E. 2001. Organic phosphorus mineralization studies using isotopic dilution techniques. Soil Science Society of
America Journal 65: 780– 787.
Özacar M. 2003. Equilibrium and kinetic modelling of adsorption of phosphorus on calcined alunite. Adsorption 9: 125 –132.
Peng SB, Eissenstat DM, Graham JH, Williams K, Hodge NC. 1993.
Growth depression in mycorrhizal citrus at high-phosphorus supply: analysis of carbon costs. Plant Physiology 101: 1063–1071.
Perrott KW, Sarathchandra SU, Waller JE. 1990. Seasonal storage and
release of phosphorus and potassium by organic matter and the microbial
biomass in a high-producing pastoral soil. Australian Journal of Soil
Research 28: 593– 608.
Pitts RJ, Cernac A, Estelle M. 1998. Auxin and ethylene promote root hair
elongation in Arabidopsis. The Plant Journal 16: 553 –560.
Raghothama KG. 2005. Phosphorus and plant nutrition: an overview. Sims
JT, Sharpley AN. eds. Phosphorus: agriculture and the environment.
Madison, WI: American Society of Agronomy, 355– 378.
Richardson AE. 1994. Soil microorganisms and phosphorus availability. In:
Pankhurst CE, Double BM, Gupta VVSR, Grace PR. eds. Soil biota:
329
management in sustainable farming systems. Wallingford: CSIRO
Publishing, 50– 62.
Richardson AE. 2001. Prospects for using soil microorganisms to improve the
acquisition of phosphorus by plants. Australian Journal of Plant
Physiology 28: 897– 906.
Richardson AE, George TS, Hens M, Simpson RJ. 2005. Utilization of soil
organic phosphorus by higher plants. In: Turner BL, Frossard E, Baldwin
DS. eds. Organic phosphorus in the environment. Wallingford, UK: CAB
International, 165–184.
Richardson AE, Hocking PJ, Simpson RJ, George TS. 2009a. Plant
mechanisms to optimise access to soil phosphorus. Crop and Pasture
Science 60: 124 –143.
Richardson AE, Barea J-M, McNeill AM, Prigent-Combaret C. 2009b.
Acquisition of phosphorus and nitrogen in the rhizosphere and plant
growth promotion by microorganisms. Plant and Soil 321: 305 –339.
Robinson D. 2005. Integrated root responses to variations in nutrient supply.
In: BassiriRad H. ed. Nutrient acquisition by plants: an ecological perspective. Berlin: Springer-Verlag, 43– 62.
Rodriguez H, Fraga R. 1999. Phosphate solubilizing bacteria and their role in
plant growth promotion. Biotechnology Advances 17: 319 –339.
Rubio G, Walk T, Ge ZY, Yan XL, Liao H, Lynch JP. 2001. Root gravitropism and below-ground competition among neighbouring plants: a modelling approach. Annals of Botany 88: 929–940.
Rubio G, Liao H, Yan XL, Lynch JP. 2003. Topsoil foraging and its role in
plant competitiveness for phosphorus in common bean. Crop Science 43:
598–607.
Runge-Metzger A. 1995. Closing the cycle: obstacles to efficient P management for improved global security. In Teissen H. ed. Phosphorus in the
global environment: transfers, cycles and management. Chichester:
Wiley, 27–42.
Ryan MH, Graham JH. 2002. Is there a role for arbuscular mycorrhizal fungi
in production agriculture? Plant and Soil 244: 263– 271.
Ryan PR, Delhaize E, Jones DL. 2001. Function and mechanism of organic
anion exudation from plant roots. Annual Review of Plant Physiology and
Plant Molecular Biology 52: 527–560.
Ryan PR, Dessaux Y, Thomashow LS., Weller DM. 2009. Rhizosphere engineering and management for sustainable agricultrue. Plant and Soil
321: 363 –383.
Sanchez PA, Shepherd KD, Soule MJ, Place FM, Buresh RJ. 1997. Soil
fertility replenishment in Africa: an investment in natural resource
capital. In: Buresh RJ, Sanchez PA, Calhoun F. eds. Replenishing soil fertility in Africa. Madison, WI: Soil Science Society of America, 1–46.
Seeling B, Zasoski RJ. 1993. Microbial effects in maintaining organic and inorganic solution phosphorus concentrations in a grassland topsoil. Plant
and Soil 148: 277– 284.
Simpson JR, Pinkerton A. 1989. Fluctuations in soil-moisture and plant
uptake of surface applied phosphate. Fertilizer Research 20: 101–108.
Smith SE, Read DJ. 2008. Mycorrhizal symbiosis, 3rd edn. London:
Academic Press.
Smith SE, Smith FA, Jakobsen I. 2003. Mycorrhizal fungi can dominate
phosphate supply to plants irrespective of growth responses. Plant
Physiology 133: 16– 20.
Snapp SS, Lynch JP. 1996. Phosphorus distribution and remobilization in
bean plants as influenced by phosphorus nutrition. Crop Science 36:
929–935.
Steingrobe B, Schmid H, Claassen N. 2001. Root production and root mortality of winter barley and its implication with regard to phosphate acquisition. Plant and Soil 237: 239– 248.
Striker GG, Insausti P, Grimoldi AA, Leon RJC. 2006. Root strength and
trampling tolerance in the grass Paspalum dilatatum and the dicot
Lotus glaber in flooded soil. Functional Ecology 20: 4– 10.
Striker GG, Insausti P, Grimoldi AA, Vega AS. 2007. Trade-off between
root porosity and mechanical strength in species with different types of
aerenchyma. Plant, Cell & Environment 30: 580–589.
Stutter MI, Shand CA, George TS, et al. 2012. Recovering phosphorus from
soil: a root solution? Enviromental Science and Technology 46:
1977– 1978.
Tarafdar JC, Jungk A. 1987. Phosphatase activity in the rhizosphere and its
relation to the depletion of soil organic phosphorus. Biology and Fertility
of Soils 3: 199–204.
Tarafdar JC, Yadav RS, Meena SC. 2001. Comparative efficiency of acid
phosphatase originated from plant and fungal sources. Journal of Plant
330
Brown et al. — Root hair ideotypes for future agroecosystems
Nutrition and Soil Science – Zeitschrift fur Pflanzenernahrung und
Bodenkunde 164: 279–282.
Tester M, Langridge P. 2010. Breeding technologies to increase crop production in a changing world. Science 327: 818– 822.
Ticconi CA, Abel S. 2004. Short on phosphate: plant surveillance and countermeasures. Trends in Plant Science 9: 548–555.
Tiessen H. 2008. Phosphorus in the global environment. In: White PJ,
Hammond JP. eds. The ecophysiology of plant– phosphorus interactions.
Dordrecht: Springer, 1– 7.
Tinker PB, Nye PH. 2000. Solute movement in the rhizosphere. Oxford:
Oxford University Press.
Turner BL, Papházy MJ, Haygarth PM, McKelvie ID. 2002. Inositol phosphates in the environment. Philosophical Transactions of the Royal
Society, London: Series B 357 449–469.
Vance CP, Uhde-Stone C, Allan DL. 2003. Phosphorus acquisition and use:
critical adaptations by plants for securing a nonrenewable resource. New
Phytologist 157: 423–447.
Van der Werf A, Welschen R, Lambers H. 1992. Respiratory losses increase
with decreasing inherent growth rate of a species and with decreasing
nitrate supply: a search for explainations for these observations. In:
Lambers H, Van der Plas L. eds. Molecular, biochemical, and physiological aspects of plant respiration. The Hague: SPB Academic
Publishing.
Veneklaas EJ, Lambers H, Bragg J, et al. 2012. Opportunities for improving
phosphorus-use efficiency in crop plants. New Phytologist 195: 306–320.
Wang L, Liao H, Yan X, Zhuang B, Dong Y. 2004. Genetic variability for
root hair traits as related to phosphorus status in soybean. Plant and
Soil 261: 77–84.
White PJ, Brown PH. 2010. Plant nutrition for sustainable development and
global health. Annals of Botany 105: 1073–1080.
White PJ, Hammond JP. 2008. Phosphorus nutrition of terrestrial plants. In:
White PJ, Hammond JP. eds. The ecophysiology of plant– phosphorus
interactions. Springer: Dordrecht, 51–81.
White PJ, Hammond JP. 2009. The sources of phosphorus in the waters of
Great Britain. Journal of Environmental Quality 38: 13–26.
White PJ, Broadley MR, Greenwood DJ, Hammond JP. 2005. Genetic
modifications to improve phosphorus acquisition by roots In:
Proceedings 568. York: International Fertiliser Society.
White PJ, Broadley MR, Gregory PJ. 2012. Managing the nutrition of plants
and people. Applied and Environmental Soil Science 2012: 104826. http://
dx.doi.org/10.1155/2012/104826.
Williamson LC, Ribrioux S, Fitter AH, Leyser HMO. 2001. Phosphate
availability regulates root system architecture in Arabidopsis. Plant
Physiology 126: 875– 882.
Wouterlood M, Cawthray GR, Turner S, Lambers H, Veneklaas EJ. 2004.
Rhizosphere carboxylate concentrations of chickpea are affected by genotype and soil type. Plant and Soil 261: 1– 10.
Yan XL, Lynch JP, Beebe S. 1995. Genetic variation for phosphorus efficiency of common bean in contrasting soil types. I. Vegetative response.
Crop Science 35: 1086–1093.
Yi K, Wu Z, Zhou J, et al. 2005. OsPTF1, a novel transcription factor
involved in tolerance to phosphate starvation in rice. Plant Physiology
138: 2087– 2096.
Zhu JM, Lynch JP. 2004. The contribution of lateral rooting to phosphorus
acquisition efficiency in maize (Zea mays) seedlings. Functional Plant
Biology 31: 949– 958.
Zhu JM, Zhang CC, Lynch JP. 2010. The utility of phenotypic plasticity of
root hair length for phosphorus acquisition. Functional Plant Biology, 37:
313– 322.
Zobel RW. 1992. Root morphology and development. Journal of Plant
Nutrition 15: 677–684.