Rethinking Internal Phosphorus Utilization Efficiency

C H A P T E R

F I V E

Rethinking Internal Phosphorus Utilization Efficiency: A New Approach Is Needed to Improve PUE in Grain Crops Terry J. Rose* and Matthias Wissuwa† Contents 1. Introduction 2. Defining PUE: Terms, Units, and Assumptions 2.1. Criteria with agronomic implications 2.2. Criteria with physiological implications 2.3. Defining the utilization of P as “efficiency” 3. Quantifying PUE of Crop Genotypes Using Criteria with Physiological Implications 3.1. Screening for vegetative PUE 3.2. Screening for grain PUE 4. P-Stress Levels in Screening Studies and the Utility of PUE in Low, Medium, and High P Input Systems 4.1. P-deficient crops suffer a range of stress levels 4.2. What are the likely outcomes of improved PUE in P-deficient plants? 5. Mechanisms and Physiology of PUE 5.1. Remobilization and scavenging of P 5.2. Alternative glycolytic pathways and mitochondrial electron transport pathways 5.3. Exploiting P-deficiency stress response mechanisms 6. Conclusions and Future Prospective 6.1. PAE versus PUE—Does one offer better chances of success? 6.2. Screening methods, targets, and possible results 6.3. Marker-assisted selection—A paradigm shift in breeding suited for PUE 6.4. Remaining questions References

186 189 189 192 195 196 197 200 201 201 202 205 205 206 206 208 208 208 209 210 211

* Southern Cross Plant Science, Southern Cross University, Lismore, NSW, Australia Japan International Research Center for Agricultural Sciences (JIRCAS), Crop Production and Environment Division, Ohwashi, Tsukuba, Ibaraki, Japan

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Advances in Agronomy, Volume 116 ISSN 0065-2113, DOI: 10.1016/B978-0-12-394277-7.00005-1

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2012 Elsevier Inc. All rights reserved.

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186

Terry J. Rose and Matthias Wissuwa

Abstract Grain crops are a key driver of the current global phosphorus (P) cycle through their continued demand for P fertilizer, and the subsequent removal of P from fields in the harvested grain. Breeding crops that can yield well with fewer P inputs (i.e., P-efficient crops) may reduce the impact of grain crops of the P cycle, but to date breeding P-efficient cultivars has focused on enhancing P acquisition efficiency (PAE). While the literature abounds in reported genotypic differences in internal P utilization efficiency (PUE) across a range of crops, there has been little progress in breeding crop cultivars with high PUE. This review critically analyzes why drawing conclusions from the body of research on PUE over the past few decades remains difficult and how progress in breeding crop cultivars high in PUE has been impeded. Four aspects of research on PUE are highlighted as being critical in limiting our understanding and exploitation of PUE in grain crops: (i) poor definition of PUE and inconsistent use of terminology, (ii) inappropriate methods used in genotypic screening for PUE that fail to account for the confounding effects of PAE on PUE, (iii) inadequate discussion on the level of P stress suffered by plants and its influence on potential mechanisms conferring high PUE and their utility in cropping systems, and (iv) a focus on P-stress response mechanisms rather than mechanisms conferring genotypic P-tolerance when investigating PUE. These factors are discussed in detail and new approaches and future areas of research on PUE are proposed.

1. Introduction Phosphorus (P) is the second most limiting macronutrient to plant growth and lack of plant-available P constrains plant growth in over 5.7 billion ha of land worldwide (Batjes, 1997). Large amounts of soil P are “locked up” in recalcitrant organic P fractions or nonlabile inorganic P pools in complexes with iron/aluminum in acid soils or with calcium in alkaline soils. While application of phosphorus fertilizer can overcome these constraints, the lack of locally available P fertilizer sources and the high cost of importing and transporting P fertilizers typically prevent resource-poor farmers in developing countries from doing so (Wissuwa and Ae, 2001). Even in Western countries where food and fiber production relies heavily on the application of nonrenewable P fertilizers, much of this fertilizer is gradually rendered unavailable to plants over time as it reacts with soil constituents (Richardson et al., 2011). In addition to P immobilization in soils, a second frequently overlooked factor is that the demand for P fertilizer is further driven by the removal of almost 10million tons of P across the globe each year in harvested produce (Lott et al., 2000), with grain crops (cereals, oilseeds, and pulses) being responsible for the vast majority of this P removal at harvest (Lott et al., 2002). Estimates suggest that as much as 85% of P applied as fertilizer can be

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removed from fields in harvest product each year (Lott et al., 2009), though regional imbalances in P budgets are apparent such that excess P inputs are applied in many areas while 30% of the globe suffer from deficits in P budgets (MacDonald et al., 2011). This inefficiency of P use in agriculture has been highlighted in many recent reviews because of environmental concerns regarding P from field runoff and human waste entering waterways and because finite global rock phosphate reserves are being depleted (e.g., Cordell et al., 2009; Richardson et al., 2011; Shen et al., 2011). Improving the P efficiency of farming systems (higher crop yields per unit of P fertilizer applied) can be achieved using agronomic strategies, for example, increasing P fertilizer availability to crops using liquid fertilizers (Holloway et al., 2001) or strategic fertilizer placement (Ma et al., 2009). In addition, breeding P-efficient crop cultivars has been advocated for improving the P efficiency of cropping systems because it is relatively low cost and, unlike optimizing fertilizer formulations and application strategies, it can provide benefits both in high-input systems and in low-input systems where fertilizer application may be rare or nonexistent due to its high cost (Rose et al., 2010). Scope also exists to breed more P-efficient cultivars because modern cultivars are generally not highly efficient at acquiring and utilizing P, having been bred under optimal conditions that selected against P-efficiency traits often present in landrace genotypes (Wissuwa et al., 2009). Traits that confer P efficiency have typically been divided into those that improve P acquisition efficiency (PAE) from soils or those that enhance (internal) P utilization efficiency (PUE) (Wang et al., 2010). However, to the best of our knowledge, all advances in breeding P-efficient grain crop cultivars have involved the exploitation of PAE traits (Wissuwa et al., 2009), and the genetics and mechanisms conferring PAE have been widely reviewed elsewhere (Hinsinger, 2001; Ramaekers et al., 2010; Shen et al., 2011; Vance et al., 2003). In contrast, PUE is poorly understood, despite a plethora of studies reporting variation in PUE among grain crop genotypes (Table 1), the mapping of several QTLs for PUE in a range of grain crops (Chen et al., 2009; Hammond et al., 2009; Su et al., 2006, 2009; Wissuwa et al., 1998; Yang et al., 2011), and discussion on PUE in many reviews on P efficiency (Ahmad et al., 2001; Batten, 1992; Richardson et al., 2011; Shen et al., 2011; Shenoy and Kalagudi, 2005; Vance et al., 2003; Wang et al., 2010). A number of factors have contributed to our poor understanding of PUE and lack of advances in breeding crops with enhanced PUE. First and foremost, PUE is not clearly defined. Typically, PUE is expressed as biomass per unit P, but biomass may refer to entire plant biomass or just grain yield, whereas the unit P may refer to fertilizer P applied, P taken up by a plant, or P present in specific tissues. The lack of a single definition being adopted across studies has made it difficult to draw conclusions from the literature. Second, PUE has long been the “‘poor cousin” in studies on P efficiency, typically investigated as an additional component in studies primarily

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Table 1 Summary of studies that have reported differences in PUE of grain crop genotypes Crop

Authors

Go´rny (1999) and Ro¨mer and Schenk (1998) Akhtar et al. (2008, 2009), Aziz et al. (2006), Duan et al. (2009), Hammond et al. (2009), and Yang et al. (2011) Common bean Arau´jo et al. (1997) and Fageria and da Costa (2000) Faba bean Stelling et al. (1996) and T. Rose (unpublished data) Maize Chen et al. (2009), Corrales et al. (2007), Fageria and Baligar (1997a), and Parentoni and Ju´nior (2008) Pigeon pea Adu-Gyamfi et al. (1989) and Subbarao et al. (1997) Rice Aziz et al. (2005), Fageria and Baligar (1997b), Fageria et al. (1988), Gill et al. (2002), Hafeez et al. (2010), Hedley et al. (1994), Saleque et al. (1998), Sahrawat et al. (1997), and Wissuwa and Ae (2001) Triticale Oracka and Lapinski (2006) Wheat Batten (1986), Batten and Khan (1987), Cao et al. (2009), Fageria and Baligar (1999), Gill et al. (2004), Go´rny and Garczy nski (2008), Gunes et al. (2006), Jones et al. (1989, 1992), Korkmaz et al. (2009), Manske et al. (2001, 2002), Osborne and Rengel (2002a,b), Ozturk et al. (2005), Sepehr et al. (2009), Su et al. (2006, 2009), Wang et al. (2005), and Yaseen and Malhi (2009a) Soybean Furlani et al. (2002), Kakar et al. (2002), Li et al. (2005), and Zhang et al. (2009) Barley Canola

designed to assess PAE and because of this, screening methodologies have not always been appropriate. Advancing our understanding of PUE has been further hampered by a failure to acknowledge and discuss the implications of the level of P in screening media and the subsequent degree of stress that plants experience. Finally, there has been a disproportionate focus on molecular research characterizing P-stress responses of individual genotypes (including mutants), as opposed to exploring loci conferring higher genotypic PUE in crop germplasm. Consequently, it remains to be seen whether exploitable genetic variation exists for those few genes and mechanisms that have so far been implicated in efficient internal P utilization (PariascaTanaka et al., 2009). These factors are the focus of discussion in this review, which places emphasis on PUE in grain crops because of their overriding influence on the global P cycle. Throughout this review, our basic premise is that PUE deserves most attention in plants experiencing some degree of P deficiency, as efficient use of P will be most important if P limits growth. Implication

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across a broader range of P supply will be discussed briefly. A second premise of this review is that the most achievable means by which to improve the PUE of modern crop cultivars is, at present, to identify loci and superior alleles within germplasm and use marker-assisted introgression to breed high-yielding varieties with specific PUE traits/genes. With that goal in mind, less emphasis is placed on PUE traits in noncultivated plants that have high PUE such as Banksia sp. (Denton et al., 2007) or stress response genes/mechanisms that are upregulated under P-deficiency stress in single genotypes of model species such as Arabidopsis (Morcuende et al., 2007) but are not necessarily differentially regulated among genotypes that differ in P efficiency (Pariasca-Tanaka et al., 2009).

2. Defining PUE: Terms, Units, and Assumptions Criteria describing the P efficiency of plants have long suffered from poor definition (Gourlay et al., 1994; Jones et al., 1989), and similarly, multiple definitions exist for terms quantifying the internal PUE of plants (Table 2). In addition, many terms and acronyms (e.g., PUE, P-efficiency ratio (PER)) are used by various authors to refer to different criteria (Table 2). To further complicate matters, the same acronym can have multiple meanings beyond measurements of internal PUE: for example, the acronym PUE is also used to refer to P uptake efficiency ( Jones et al., 1992) or P use efficiency (grain yield per soil available P; Parentoni and Ju´nior, 2008). This range of definitions and lack of consistent terminology for a given criterion are undoubtedly responsible for some apparent contradictions in the literature and has made drawing conclusions difficult. In this review, PUE is defined as the biomass produced per unit P accumulated in tissue (gtissueDMmg
1 tissue P), and the grain yield per unit of P accumulated in aboveground plant material is referred to as the PER (ggrainDMmg
1 shoot P). The criteria used to quantify various aspects of internal PUE can be broadly classified into those that have agronomic relevance and those that have physiological relevance. Criteria that measure grain yield as a component evidently have agronomic implications with PER or the “critical shoot P concentrations for 90% maximum yield” being typical examples, whereas on face value PUE (gDMmg
1 P) measurements have little direct agronomic application.

2.1. Criteria with agronomic implications Citing the trend of increasing average global grain yields over the past half a century, it is possible to argue that PER has been selected for and improved in modern crop varieties (Hammond et al., 2009). Indeed,

Table 2

Definitions of criteria used to assess phosphorus utilization efficiency in literature

Criterion definition and units

Terminology

Authors

Batten (1992) and Jones et al. (1992) Parentoni and Ju´nior (2008) Ro¨mer and Schenk (1998) Kakar et al. (2002) Yaseen and Malhi (2009a) Ahmad et al. (2001) Manske et al. (2001, 2002) Shoot dry matter per unit P Gourlay et al. (1994) and Yaseen and Malhi accumulated (g DM mg
1 P) (2009b) Internal phosphorus utilization efficiency (PUE) Rose et al. (2011) Phosphorus utilization efficiency (PUE) Oracka and Lapinski (2006) and Osborne and Rengel (2002a,b) Phosphorus utilization efficiency (PUTE) Sepehr et al. (2009) Shoot DM/shoot P Phosphorus utilization index (PUI) Yaseen and Malhi (2009b) concentration (g2 DM mg
1 P) Phosphorus utilization efficiency (PUE) Go´rny (1999), Gourlay et al. (1994), and Siddiqi and Glass (1981) Physiological phosphorus use efficiency (PPUE) Hammond et al. (2009) Tissue P concentration required Chen et al. (2009) and White and for 90% maximum yield Hammond (2008) Grain yield per unit of P accumulated in shoots at maturity (kg grain g
1 P)

P-efficiency ratio (PER) P internal utilization efficiency (PUTIL) P utilization efficiency quotient (PEQ) P utilization efficiency (PUE) P physiological efficiency index (PPEI) Physiological P use efficiency (PPUE) Phosphorus utilization efficiency (PUTE) P-efficiency ratio (PER)

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modern varieties (MVs) of rice typically had higher PERs than traditional or landrace cultivars in an upland (aerobic) screening trial: however, the PER was significantly correlated to harvest index (HI) such that the low PER of many traditional varieties simply reflected their much lower HI and grain yield potential (T. Rose and M. Wissuwa, unpublished data). Similarly, studies with wheat also concluded that PER was more highly correlated to HI than with grain yield (Batten and Khan, 1987). Perhaps the most telling study was that of Manske et al. (2002): these authors studied a number of P-efficiency traits in near isogenic wheat lines differing in dwarfing characteristics and showed that the yield-increasing effect of two dwarfing genes led to higher PER. Thus, the apparent improvements in PER in MVs often reflect their higher HI rather than specific selection of physiological traits that improve internal P utilization in plants. Calculating the tissue P concentration required for a given percentage of maximal grain yield, referred to as the “critical” tissue P concentration if this is 90% of maximal yield (White and Hammond, 2008), avoids the issue of confounding P efficiency with HI because HI becomes inconsequential when the yield of a genotype is expressed as a percentage of its own maximum yield. However, this criterion may only be useful when all genotypes screened have a similar yield potential: comparing the critical tissue P concentration of a landrace with low yield potential (e.g., 4tha
1) to that of a high-yielding MV (e.g., 8tha
1) is likely to produce misleading results that may favor low-yielding genotypes. A further issue with using grain yield as a parameter in defining internal PUE, either as PER or as “critical” tissue P concentration, is that yield formation not only depends on the yield potential of a given genotype but also equally on location-specific effects such as day length, temperature, or disease pressure. Thus, while critical tissue P concentrations and PER could be used in breeding nurseries to evaluate locally adapted highyielding breeding lines, neither criterion would be suitable to evaluate P efficiency across a broad range of genotypes. Further, it remains questionable whether sufficient genetic variation exists for these P-efficiency traits among a set of rather similar breeding lines that have typically been developed in well-fertilized nurseries (Wissuwa et al., 2009). Ideally, screening studies investigating internal P utilization traits should maximize the portion of the gene pool assessed within a crop species in search of novel genes/alleles, many of which may only be present in older varieties that were developed prior to the widespread use of P fertilizers. To enable valid comparisons of older varieties and MVs, and to investigate physiological mechanisms, it would be preferable to define PUE as the biomass produced per unit P accumulated in tissue (gDMmg
1 P) and to dissect PUE into components such as grain PUE, shoot PUE, and root PUE and look to improve them individually.

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2.2. Criteria with physiological implications 2.2.1. PUE at the vegetative stage PUE has typically referred to shoot PUE (shoot dry weight per unit of P in shoot) and occasionally root PUE, and both have been quantified across a range of species (Table 1). Reported shoot P concentrations (the inverse of PUE) range from below 1 to above 10mgPg
1 DM, depending on the species and level of P supply (Table 3). The range of P concentrations observed in roots tends to be narrower than in shoots, and root P concentrations are typically lower than corresponding shoot P concentrations across most crop species (Table 3), possibly implying that roots have a lower “P cost of production.” However, interpreting root PUE on a P investment per unit DM basis may be misleading because ultimately, the volume of soil explored by roots for P acquisition is driven by root length (or surface area) rather than root biomass (the denominator when calculating root PUE). If root PUE was defined as mm2 root surface area mg
1 P, then screening for root attributes known to increase root length with minimal P investment such as root fineness, cortical aerenchyma, or root hair formation (Lynch and Ho, 2005) may be more fruitful than screening for lower root P concentrations per se. A study in maize reported that an acknowledged P-efficient genotype had lower root P concentration in lateral roots in addition to higher specific root length than a P-inefficient genotype (Zhu and Lynch, 2004). It may therefore be possible to combine the desired root traits mentioned above with mechanisms that allow roots to function at a lower P concentration (i.e., high PUE). Further, data presented by Rose et al. (2011) suggest that control of root PUE and shoot PUE is genetically independent, so selecting for both traits should be possible. Investigating genotypic differences in tissue-specific PUE would ideally lead to the identification and selection of favorable alleles that confer increased biomass production per unit P within each tissue studied. Preliminary results with rice suggest that such loci may differ between root and shoot (Rose et al., 2011) and possible mechanisms are discussed in Section 5. The validity of approaches focusing on screening for vegetative PUE has been questioned based on the absence of direct evidence linking vegetative PUE to improved grain yield (e.g., Siddiqi and Glass, 1981); however, as outlined above, the absence of such a positive link might be expected, given confounding effects of HI and yield potential. What would be of concern is a negative association between vegetative PUE and grain yield, but we are unaware of any data suggesting such association. In fact, in rice, high-yielding cultivars were represented among the highest and lowest ranked genotypes for shoot PUE (Rose et al., 2011). The relationship between shoot PUE and grain yield is nonetheless critical, and the identification of loci conferring high PUE in crops should facilitate further research in this area.

Table 3

Variation in shoot and root PUE (expressed as tissue P concentrations) during vegetative growth of three major grain crops P concentration (mg P g
1 DM)

Crop

Wheat

Plant age (DAS)

Shoots

Roots

Reference

29

1.04 (low P) 4.27 (medium P) 4.29 (high-P) 1.2–1.9 (low P) 2.6–5.9 (high P) 1.57–2.29 (low P) 2.80–4.49 (high P) 1.2–1.8 (low P) 1.8–2.8 (medium P) 6.9–11.9 (high P) 2.0–3.1 (low P) 3.1–6.2 (high P) 1.55–2.01 (low P) 2.53–3.76 (high P) 0.6–1.7 (low P) 4.0–12.7 (high P) 1.4–2.6 (low P) 4.1–5.9 (high P)

0.74 (low P) 1.79 (medium P) 2.19 (high P)

Fageria and Baligar (1999)

35 39 41

42 49 54 56

Osborne and Rengel (2002a) Ozturk et al. (2005) Osborne and Rengel (2002b)

3.0–6.5 (high P)

Yaseen and Malhi (2009a) Gunes et al. (2006) Korkmaz et al. (2009) Sepehr et al. (2009) (Continued)

Table 3

(Continued) P concentration (mg P g
1 DM)

Crop

Rice

Plant age (DAS)

Shoots

Roots

Reference

35 50

3.44–6.92 0.60–1.14 (low P) 2.80–4.50 (high P) 1.2 (low P) 2.2 (medium P) 2.7 (high P) 0.41–0.52 (low P) 1.94–2.53 (high P) 0.62–0.87 1.98–2.35 (low P) 7.25–8.97 (high P)

3.73–7.16 0.34–0.82 (low P) 2.03–3.61 (high P) 0.9 (low P) 1.8 (medium P) 2.0 (high P) 0.54–0.66 (low P) 1.1–1.2 (high P) 0.8–2.65 4.41–9.14 (low P) 3.54–4.02 (high P)

Hafeez et al. (2010) T. Rose et al. (unpublished)

73

Unknown Canola

40 41

Fageria et al. (1988)

Hedley et al. (1994) Aziz et al. (2006) Akhtar et al. (2009)

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2.2.2. PUE at the reproductive stage Crop P requirements in postanthesis growth are dominated by two competing processes: the P requirements of vegetative tissues to continue normal cellular function (including function throughout the senescence process in determinant crops) and the P demand of the developing grain (Rose et al., 2007). Theoretical calculations suggest that levels of P in grains are well above the P levels required for normal cellular function (Raboy, 2009), consistent with earlier physiological studies that reported that grain yield was not limited by the amount of P in the grain (Batten et al., 1986). Thus, genotypic variation in grain P levels would likely be due to reduced sink strength of the grain as a P storage organ rather than a lower physiological requirement. Reduced P sink strength of the developing grain may therefore be an ideal PUE trait in reproductive growth phases, given higher remobilization of P from vegetative tissues to grains does not improve grain yields (Batten et al., 1986) but may impair leaf function (Garcia and Hanway, 1976). While such a trait has gained recent attention (Richardson et al., 2011; Rose et al., 2010), it remains to be seen whether it can be exploited in breeding crops with high PUE and whether a certain threshold grain P concentration needs to be maintained to avoid loss in seedling vigor, particularly on low-P soils.

2.3. Defining the utilization of P as “efficiency” PUE (gDMmg
1 P) or PER (ggrainmg
1 aboveground P) are typically evaluated following the assumption that higher PUE/PER in some genotypes ultimately translates to superior biomass or grain yield. However, since PUE is defined as a ratio (gbiomassmg
1 P), a genotype “A” may show higher PUE (i) if it has proportionally higher biomass than P content compared to a genotype “B” or (ii) if it has proportionally lower P content than biomass relative to genotype “B.” Obviously case (i) is what would make genotype “A” efficient in a positive sense that could be exploited in breeding, whereas case (ii) would likely indicate a higher degree of P starvation in genotype “A” and not true PUE. Unfortunately, both cases cannot be distinguished without further examining the data beyond simple calculations of PUE and it should be strongly emphasized that such further analysis is crucial in order to avoid misinterpretations of genotypic rankings in PUE (Rose et al., 2011; Wissuwa et al., 1998). The most straightforward way of establishing whether PUE/PER values represent true efficiency is to test for a positive correlation with biomass; should the correlation be insignificant or negative, then PUE/PER values do not reflect “efficiency” per se but may indicate a higher degree of P starvation. Such negative correlations are surprisingly common (Gunes et al., 2006; Rose et al., 2011; Sepehr et al., 2009; Wissuwa et al., 1998) typically arising in screening

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Table 4 Correlation coefficients between shoot P content, biomass, and shoot PUE from four experiments conducted over a range of P supply from deficient to fully fertilized Shoot biomass

(a) Low-P soil (Wissuwa et al., 1998) P content 0.98** Biomass (b) Mildly P deficient (Rose et al., 2010) P content 0.73** Biomass (c) Fixed (low) P supply (Rose et al., 2011) P content 0.50** Biomass (d) Excess P (Rose et al., 2008) P content
0.17ns Biomass

Shoot PUE


0.72**
0.61**
0.52** 0.12ns
0.51** 0.49**
0.92** 0.52**

** denotes significant difference at P < 0.001

experiments that concurrently evaluate genotypic differences in PAE under severe or mild P deficiency (Table 4a and b). As will be discussed in more detail in following chapters, it will be necessary to adjust screening methods to avoid such “nonsensical” genotypic rankings for PUE (Table 4c).

3. Quantifying PUE of Crop Genotypes Using Criteria with Physiological Implications The above considerations regarding various definitions of PUE already indicate that evaluating PUE is not as trivial as it may seem. Screening methods would obviously differ based on the preferred definition, which, in turn, would depend on the ultimate purpose of screening. As outlined above, the potentially confounding effects of HI, yield potential, and local adaptation need to be considered and would limit screening for what we defined as agronomic PUE criteria to sets of rather homogeneous material such as high-yielding advanced breeding lines. For the identification of novel loci/genes in more broad genetic material, protocols need to be devised that allow for genotypic comparisons that are unbiased by genotypic differences in traits that are not directly related to PUE. As shall be discussed below, even for the definition of PUE deemed most suitable for this purpose, gDMmg
1 P for various plant tissues, screening methods require careful consideration.

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3.1. Screening for vegetative PUE 3.1.1. Traditional screening systems The standard method for quantifying the PUE of crop genotypes has been to screen any number of genotypes in field or glasshouse conditions and to simultaneously assess a number of P-efficiency criteria including PUE. Such studies typically use measurements of shoot biomass, grain biomass, and shoot and grain P concentrations to calculate PUE, PAE, PER, or other criteria (e.g., Hammond et al., 2009; Oracka and Lapinski, 2006; Osborne and Rengel, 2002a,b). However, we recently hypothesized that such screening systems were of limited use because PUE is strongly affected by the level of P deficiency suffered by the plant, which is directly linked to the amount of P taken up (Rose et al., 2011). This hypothesis was based on the widely reported phenomenon that PUE decreases (tissue P concentrations increase) with increasing P supply in the screening media (Fageria et al., 1988; Hedley et al., 1994; Osborne and Rengel, 2002a,b; Saleque et al., 1998). Further, this decrease is not linear (Fig. 1), which means that any additional unit P taken up would be converted to biomass slightly less efficiently. As can be derived from the data in Fig. 1, the effect of plant P content (or P uptake) on PUE is particularly pronounced under P-deficient conditions—which typically are the growth conditions where genetic improvements in PUE would be most welcome and, hence, where precise genotypic evaluations are crucially important. Should genotypes to be evaluated for PUE be screened in a system that simultaneously allows for genotypic differences in PAE to be expressed, it is likely that such differences in PAE would confound any difference in PUE, given the nonlinear relation between both parameters. Results from QTL mapping experiments confirm this direct link between PUE and P uptake (PAE), since QTL for PUE and P uptake was mapped to the same loci, albeit with opposite genotypic effects (Yang et al., 2011). Even the Pup1 locus, the most influential QTL for P uptake identified in rice to date, was mapped to the same location as the main QTL for PUE, but whereas the Pup1 locus doubled P uptake, it strongly reduced PUE (Wissuwa and Ae, 1999). Key correlations between PUE, P content, and biomass for this QTL mapping experiment (Table 4a) confirm the negative association between PUE and P uptake. The phenotypic data of this mapping population shown in Fig. 2 thus serve to illustrate three important points, namely, (i) comparisons between genotypes that concurrently differ in P uptake do not allow for unbiased estimates of PUE, (ii) estimates of high PUE of certain genotypes may be of no practical or genetic relevance if they merely reflect a higher degree of P starvation, and (iii) defining g DM per unit P (PUE) as “efficiency” can be rather misleading if its contextual significance is ignored, that is, if the correlation between PUE and biomass is negative (Table 4a).

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2.5 y = 2.31x −0.49 R 2 = 0.96

PUE shoot (g DM mg P-1)

2.0

1.5

1.0

0.5

0.0 0

10 20 30 Shoot P content (mg plant −1)

40

Figure 1 Shoot PUE as affected by shoot P content over a wide range of P supply levels. Data presented are based on experimental data of Wissuwa et al. (2005). Briefly, the experiment compared biomass accumulation of two closely related genotypes differing for the presence of the Pup1 locus in a nutrient solution experiment under four levels of P supply (3.2, 6.4, 9.6, and 100mMP). Genotypic differences were not significant, so data from both genotypes were combined. A power function provided the best fit to the experimental data.

Other studies have assessed relationships between P-efficiency criteria in screening experiments (e.g., Hammond et al., 2009) or have attempted to determine the contribution of both PUE and PAE to overall P efficiency across genotypes (Parentoni and Ju´nior, 2008). However, given the interdependence of these variables, and the overriding impact of PAE on biomass production in screening trials on low-P soils, the results of any attempts to determine the relative contributions of PAE and PUE are questionable. 3.1.2. A modified nutrient solution screening technique to nullify differences in P uptake among genotypes To overcome the confounding influence of P uptake in screening studies, we recently developed a simple screening method in which genotypes were grown in nutrient solution in individual containers supplemented with a

199

Internal Phosphorus Utilization Efficiency in Grain Crops

4 Dry matter (g plant–1)

10

PUE (mg P g–1 DM)

3

8 6

4 2

0 0

1

2

3

4

5

6

–1

P content (mg plant )

2

1 R 2 = 0.64 0 0

1

2 3 4 P content (mg plant–1)

5

6

Figure 2 Shoot PUE as affected by shoot P content in a QTL mapping population grown on low-P soil (Wissuwa et al., 1998). Lines with the lowest P uptake appear to be most efficient in utilizing P; however, they also fail to produce adequate shoot biomass (inlay), which indicates that the apparent high PUE is due to severe P starvation and not true efficiency in a sense that could be harnessed in plant improvement.

specific low amount of soluble P to nullify the influence of P uptake (Rose et al., 2011). Nutrient solution experiments have been used repeatedly to estimate genotypic variation in shoot PUE across a range of species (Akhtar et al., 2008; Hafeez et al., 2010; Yaseen and Malhi, 2009b); however, all genotypes were typically grown in the same containers in competition for the amount of P supplied. Consequently, confounding effects due to differences in rates of P absorption among genotypes existed. This was avoided in our modified method that used individual containers per genotype with 500mgP added to each container. Twenty-nine rice genotypes were screened using this technique, resulting in variation in root PUE and shoot PUE that showed no correlation with genotypic PUE rankings of the same genotypes screened in soil (Rose et al., 2011). This study confirmed that genotypic differences in PUE do exist in the absence of large genotypic differences in PUE, and further, shoot PUE was positively correlated to biomass production (Table 4c), suggesting that efficiency of P utilization was responsible for biomass production (Rose et al., 2011).

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While this technique holds promise for screening of large numbers of rice genotypes, screening of other crop species that require aerated nutrient solution may be impractical. It is possible that PUE mechanisms/loci might be specific to certain level of P deficiency with little effects above/ below certain thresholds. It would therefore be desirable to screen at more than one level of P deficiency or at least to confirm results with selected genotypes over a range of P supplies. High PUE genotypes identified using such screening techniques would require further study in soilbased growth conditions to determine the effect of high-PUE mechanisms when feedback mechanisms between PAE and PUE exist. Another factor that affects all vegetative screening studies is the duration of plant growth, since ontogeny plays a role in the critical P requirement of plant tissues (Ahmad et al., 2001). Screening for PUE at the seedling stage may avoid this complication but plants must be grown for sufficient duration to eliminate effects of genotypic differences in seedling vigor; that is, plants must be grown for such a period of time that all plants are P deficient in order for PUE to become the primary driver of biomass production (Rose et al., 2011).

3.2. Screening for grain PUE Several studies have investigated the possibility of reducing grain P levels using criteria including the proportion of aboveground P located in the grain at maturity, or phosphorus HI or the P concentration in grains at maturity (Batten, 1992; Jones et al., 1992; Rose et al., 2010). While genotypic variation for PHI was apparent in these studies, it was strongly influenced by the HI of any given genotype and was therefore of questionable validity. Batten (1992) also reported that grain P concentration appeared to be a function of grain yield in wheat (i.e., a dilution effect whereby greater grain yield resulted in lower grain P concentration). However, we found no such correlation in a screening study with rice (Rose et al., 2010) and Stangoulis et al. (2007) mapped QTLs for rice grain P concentration in an AzucenaIR64 mapping population, suggesting that grain P is under independent genetic control to a degree. In fact, a number of studies have mapped QTLs for total grain P in the model species Arabidopsis and its crop relative Brassica rapa (Bentsink et al., 2003; Ding et al., 2010; Ghandilyan et al., 2009; Zhao et al., 2008), but what is not known is whether these QTLs coincided with either QTL for plant P uptake or grain yields. Thus, while it is possible that screening for grain PUE (grain P concentration) may be achieved using conventional screening trials with a wide range of genotypes, or mapping populations, further research is required into the extent to which plant mineral uptake and GE interactions play a role in grain P concentrations in such studies.

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4. P-Stress Levels in Screening Studies and the Utility of PUE in Low, Medium, and High P Input Systems 4.1. P-deficient crops suffer a range of stress levels The level of P stress suffered by plants in screening studies has typically varied depending on native P levels in the growing media and the amount of supplemental P fertilizer, and as such, a range of shoot and root P concentrations have emerged across screening studies to date (Table 3). Given that the critical shoot P concentration for wheat and rice is in the range of 2–5 and 1–2mgPg
1 DM, respectively, during the vegetative stage (Dobermann and Fairhurst, 2000; Reuter and Robinson, 1997), the shoot P concentrations summarized in Table 3 (ranging from 0.6 to 7–12mgPg
1 DM) represent the full range from highly P-deficient to P-replete plants, with luxury P consumption being likely toward the high end tissue P concentrations. These wide ranges reported pose the question whether the concept of PUE should be applied equally to this entire range. At the outset of the review, we stated that our primary focus is on PUE under Pdeficient conditions, defining P deficiency as a situation where an additional supply of P to the plant would increase plant biomass (in the physiological sense) or crop yield (in the agronomic sense). The focus on shoot and root PUE in P-deficient plants is justified because in plants that are not P-deficient, biomass production is typically not correlated to PUE (Rose et al., 2011) or P uptake (Table 4d). In these circumstances, any differences among genotypes tend to reflect differences in luxury uptake of P, that is, uptake of P beyond the requirements necessary for maximum biomass or grain yields. When PUE is not the causal factor for differences in biomass accumulation, measurements of g DMmg
1 P no longer represent “efficiency.” A recent review on PUE by Wang et al. (2010) concluded that PUE had a dominant influence on the P efficiency of crops at adequate and high P supply, and therefore PUE would become a bottleneck for breeding P efficiency in high-P input agriculture. However, the premise for this conclusion was that PAE had little impact in high-P conditions (because sufficient P is supplied as P fertilizer), and the paper of Manske et al. (2001) was cited as evidence for the high contribution of PUE to P efficiency in P-fertilized crops. However, the PER was not significantly positively correlated with grain yield in any of the eight treatment combinations in the study of Manske et al. (2001); hence, these measurements do not satisfy the requirements of “efficiency” as defined in Section 2.3. In contrast to the conclusion of Wang et al. (2010), we suggest that in adequate or high-P conditions, shoot or root PUE may be of limited practical relevance.

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There is, however, a strong desire to enhance the P efficiency of highly productive agricultural systems because heavy reliance on P fertilizer has led to eutrophication of water bodies due to P runoff from fields (Sharpley et al., 2001), as well as increased production costs. While enhancing shoot and root PUE may be of little benefit in high-input agriculture, improving the grain PUE may be promising for improving the P efficiency of such systems (Richardson et al., 2011; Rose et al., 2010). However, little work has been done in this field of research and its potential to improve the P efficiency of farming systems will depend on whether genetic variation can be exploited or mutant/transgenic approaches can be successfully applied, and the impact of such a trait on other grain quality attributes and agronomic traits when the grain is used as seed. While at the opposite end of the spectrum are crops grown in povertystricken nations in Africa that suffer from severe P-deficiency stress, the majority of P-deficient crops across the globe tend to suffer from a more moderate level of P-deficiency stress. One issue with the study of Rose et al. (2011) was that the level of P used to screen genotypes (one-off dose of 500m gP) resulted in severely P-deficient plants that are rarely observed in commercial rice fields. Investigating PUE in P-starved plants has also been used to elucidate P-stress response mechanisms in rice at the molecular level (Morcuende et al., 2007; Pariasca-Tanaka et al., 2009), but whether any genes upregulated or physiological mechanisms identified in such P-deficient plants have any relevance in plants suffering mild P deficiency is not known. Screening plants at a P level sufficient for production of 70–80% maximum biomass yield at a given growth stage may identify mechanisms that are active under typical field conditions, and whether such a level of stress is sufficient to allow phenotypic separation of genotypes for PUE needs to be resolved. Perhaps the most comprehensive screening approach would be to derive P response curves to allow determination of critical tissue P concentrations for any percentage of maximum shoot biomass yields. However, screening large numbers of genotypes in this fashion would be prohibitively expensive and impractical. Further studies on PUE are needed to address this issue and elucidate which mechanisms that enhance PUE operate at various P-stress levels, whether genotypic variation exists, and whether such mechanism have any impact when plants are grown in field conditions.

4.2. What are the likely outcomes of improved PUE in P-deficient plants? While identifying mechanisms and genes that enhance PUE in plants suffering from varying degrees of P-deficiency stress has proved difficult, predicting the phenotypic outcome of the exploitation of such mechanisms on the P efficiency of commercial crop cultivars is equally difficult. As discussed earlier, P uptake affects PUE and confounds PUE rankings in

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genotypic screening studies on P-deficient soils. However, modeling studies suggest that PUE also affects P uptake, either because higher root PUE would enhance root growth directly since a greater root surface area could be produced at equal P cost or because root growth is affected indirectly if higher shoot PUE allows greater P distribution to roots (Wissuwa, 2003). The theoretical outline of the model with regard to effects of changes in PUE is shown in its most simplified form in Fig. 3: an increase in root PUE of 20% would produce 20% higher root biomass and soil exploration leading to 20% more P uptake above what would have been taken up in a genotype without the PUE increase. At time txþ1, a portion of the additional P taken up remains in roots (6%, assuming 70% of P is distributed to shoots), and this additional P is also converted to root biomass at the higher internal efficiency, resulting in 27.2% higher biomass and P uptake. Over an entire cropping cycle, the effect of improving PUE would therefore be far greater than the initial “physiological” PUE differential between two genotypes

Assimilate distribution

Shoot biomass

PUE

tx : +20% tx+1: +27.2% tx+2: +29.8%

70%

Root:shoot

P uptake

P distribution 30%

tx : tx+1: +6% tx+2: +8.2%

PAE

Soil exploration

PUE

Architecture

Root biomass tx : +20% tx+1: +20% +(6*1.2)% tx+2: +20% +(8.2*1.2)%

Figure 3 Schematic outline of the principles behind the model “P-LIM-GROW,” assuming a 20% increase in PUE of roots, as indicated by 20% higher root biomass at time tx. Adapted from Wissuwa (2003) and Rose et al. (2011).

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would suggest because increased PUE would also enhance P uptake (Rose et al., 2011; Wissuwa, 2003). Small genotypic differences in PUE as detected in our modified screening experiment (Rose et al., 2011) could therefore be well worth exploiting in plant breeding, at least in P-deficient scenarios where growth is limited directly by insufficient P availability rather than by assimilate supply (Wissuwa et al., 2005). In addition to the obvious reason for focusing on PUE, the efficient use of a limited and costly resource, improving PUE rather than PAE alone may be more sustainable since relying solely on increasing P uptake would pose the danger of overmining soil-P reserves, particularly in low or zero input agricultural systems (Henry et al., 2010). The theoretical considerations put forward in Fig. 3, as well as additional experimental data on lowcost root systems and their effect on soil exploration (Zhu and Lynch, 2004), indicate that a strict separation of PUE and P uptake may be impossible since enhanced PUE, especially in roots, would also enhance P uptake and mining of soil-P. Thus, improving grain PUE is theoretically the only option for reducing the amount of P taken up by crops in P-deficient scenarios, with the added benefit of minimizing the removal of P from fields, which would be beneficial in low-input and high-input cropping systems. However, any potential reductions in P uptake by crops with high grain PUE will depend on whether a reduction in competition for P between the grain and vegetative tissues triggers a decline or cessation in P uptake from soil. Research to date has produced no firm conclusions: for example, early work suggested that wheat crops acquire sufficient P for maximum grain yields by anthesis (Batten et al., 1986; Boatwright and Viets, 1966), yet studies have shown that wheat plants may cease (net) soil uptake at anthesis, accumulate small additional amounts of P beyond anthesis, or take up a substantial proportion of total plant P after anthesis (Manske et al., 2002; Mohamed and Marshall, 1979; Ro¨mer and Schilling, 1986; Rose et al., 2007) and this pattern is genotype specific ( Jones et al., 1992). Indeterminate crops such as canola, or crops that are partially perennial such as rice, continue to acquire P from the soil during grain filling to satisfy the competing demands of actively growing vegetative tissue and the developing grain (Rose et al., 2009, 2010). Thus, it is unclear whether determinate or indeterminate crop species (or genotypes within crop species) would reduce their net P uptake if postanthesis P demand was reduced. Whether regulatory mechanisms exist that reduce P uptake from soils when P demand has been satisfied during postanthesis growth is therefore a key question that remains to be addressed in future research. Interestingly, among the suite of mutants with reduced phytic acid levels in grains (lpa mutants) developed over the past decade, one barley lpa mutant also has lower total grain P (Raboy, 2009). However, to the best of our knowledge, it is not known whether this mutant has lower postanthesis P uptake from soil compared to wild-type barley plants.

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5. Mechanisms and Physiology of PUE Most of our knowledge on plant adaptation to P-deficiency stress pertaining to internal P utilization has emerged from studies that have examined the physiological or transcriptional changes that occur in single genotypes of a species that have been subjected to P stress. As with genotypic screening studies, the range of P deficiency suffered by plants in such studies has varied from severely P-deficient plants grown for weeks in a P-deficient soil (Pariasca-Tanaka et al., 2009) to plants under less severe P stress that were grown in optimum (200mM) P solution before being transferred to low-P nutrient solution for 1–10 days (Caldero´n-Va´zquez et al., 2008). The duration or severity or P stress determines both the number of type of genes that are up- or downregulated as in response to this stress (Hammond et al., 2003; Pariasca-Tanaka et al., 2009).

5.1. Remobilization and scavenging of P A major plant adaptation to P-deficiency stress is the enhanced remobilization and recycling of P in plant tissues. Under P-replete conditions, the vast majority of Pi is stored in vacuoles with only 5–15% of Pi in the cytoplasmic pool, and in the early stages of P deficiency, inorganic P is redistributed from the vacuoles to the cytoplasm to maintain minimum cytosolic P levels (Raghothama and Karthikeyan, 2005). However, recent work suggests that during P starvation Pi efflux from the vacuole cannot compensate for a rapid decrease of the cytosolic Pi concentration, and this sudden drop may be the first endogenous signal triggering the Pi starvation response (Pratt et al., 2009). As P starvation sets in, both inorganic P and P remobilized from organic compounds are redistributed from older tissues to metabolically active tissues including growing points and young leaves and active roots (Akhtar et al., 2008). Membrane lipid composition may be altered to reduce consumption of P, and degradation of existing phospholipids into Pi and diacylglycerol is a key process in the remobilization of P during P starvation (Li et al., 2006). Because P is a key component of nucleic acids, phospholipids and metabolites of energy-mediated metabolic processes, phosphatases, ribonucleases, and several key genes involved in lipid metabolism including phospholipase, UDP-sulfoquinovose synthase (SQD1), and sulfoquinovosyldiacylglycerol (SQD2) are among those that are strongly upregulated under P-deficiency stress (Caldero´n-Va´zquez et al., 2008; Pariasca-Tanaka et al., 2009). Increased expression of putative Pi-transporters would then allow for rapid redistribution of the P remobilized by above processes (Vance et al., 2003). Interestingly, while it is generally thought that upregulation of genes such as Pi-transporters will improve PUE, in the case of grain PUE, the opposite

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may be the case because a reduction in translocation of P to the developing grain is desirable (Rose et al., 2010). Thus, reduced expression of high-affinity Pi-transporters in reproductive tissues may result in a decrease in grain P levels and enable continual utilization of P in photosynthetic tissues (Lambers et al., 2006).

5.2. Alternative glycolytic pathways and mitochondrial electron transport pathways Several enzymes of the glycolytic pathway are Pi dependent, but in plants suffering P-deficiency stress Pi-dependent or adenosine-tri-phosphate (ATP)-dependent steps can be bypassed (Theodorou and Plaxton, 1996). Similarly, alternative mitochondrial electron transport pathways can be utilized that bypass the adenylate and Pi reaction (Theodorou and Plaxton, 1993). For detailed discussion on the various alternative pathways and the enzymes involved, the reader is referred to reviews by Theodorou and Plaxton (1993) and Vance et al. (2003). In addition to the physiology of alternative glycolytic and respiratory pathways, much information regarding the genes involved in these processes has been gleaned from transcriptomics studies on P-deficient plants. In particular, genes such as phosphofructokinase (PFK), pyrophosphate: fructose-6-phosphate phosphotransferase (PFP), pyruvate kinase, and phosphoenolpyruvate carboxylase (PEPC) have been implicated in modifications to carbon metabolism that bypass P-requiring steps (Hammond et al., 2004; Pariasca-Tanaka et al., 2009). In addition, a multitude of genes are involved in regulating the above responses to P stress (Hammond et al., 2004). There are a multitude of genes and physiological processes that are affected by P-deficiency stress, and these have been the subject of a number of review papers over recent years (Ahmad et al., 2001; Caldero´n-Va´zquez et al., 2011; Hammond et al., 2004; Shen et al., 2011; Shenoy and Kalagudi, 2005; Vance et al., 2003; Wang et al., 2010), and the reader is referred to these reviews for detailed discussions. In this review, we focus on the key question as to whether these genes can potentially be manipulated to improve the PUE of grain crop cultivars.

5.3. Exploiting P-deficiency stress response mechanisms Attempts have been made to enhance the PAE of crop cultivars through the overexpression of genes that are responsive to P-deficiency stress, but to date, the results have not been entirely promising. For example, transgenic plants that have enhanced phytase exudation can effectively access organic P sources in artificial conditions, but their usefulness in field situations is limited (George et al., 2005). Similarly, overexpression of high-affinity P transporters did not enhance P uptake rates from soil (Rae et al., 2004) and

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overexpression of genes related to the synthesis of organic acids has not yet proved to be a successful strategy for increasing the PAE of plants (summarized in Richardson et al., 2011). Similarly, the known genetic and physiological responses of plant to P-deficiency stress related to PUE have yet to have made the leap from the laboratory to the field. As yet, we are unaware of any studies that have conclusively shown that the overexpression of any P-stress response genes confers higher PUE in plants. Wang et al. (2009) overexpressed an Arabidopsis purple acid phosphatase gene (AtPAP15) in soybean and reported higher yields in the transgenic plants when grown on a low-P acid soil, and concluded that higher internal PUE was the likely cause. However, no data on P uptake by plants or tissue P concentrations were presented, and in earlier experiments, the transgenic plants showed greater phytase secretion from roots and enhanced P acquisition from organic P sources; hence, improved P uptake may have been the causal factor in yield differences. The lack of progress in improving P efficiency through manipulation of genes that are responsive to P stress suggests that in many instances P-stress response mechanisms are not necessarily those that confer tolerance to P stress. A microarray study comparing a P-efficient rice near isogenic line containing the Pup1 locus with its P-inefficient parent Nipponbare came to similar conclusions with regard to many PUE stress response genes (Pariasca-Tanaka et al., 2009). While many of the aforementioned PUE-related genes were upregulated in root and shoot tissue, virtually all were induced to a similar or higher degree in the P-inefficient Nipponbare than the P-efficient NIL6-4 (Pariasca-Tanaka et al., 2009). Thus, even genotypes that show poor tolerance to P deficiency in the field have evolved many of the well-known adaptations to P stress. Questions remain as to whether the manipulation of P-stress response genes using biotechnology can facilitate improvements in the PUE of field-grown crops, but given the rate at which global P resources are being depleted, further research is warranted. In terms of breeding crops higher in PAE, the most promising option to date has been to exploit natural variation among genotypes (Lynch, 2007; Wissuwa et al., 2009). It is therefore surprising that although the physiological and molecular responses to P stress have been widely studied, little is known regarding mechanisms that confer higher PUE in genotypes of the same species. While there still remains much to be elucidated about the genetics and physiology of P-stress responses, further research also needs to target the identification of valid QTLs from appropriate screening studies to determine the genes and mechanisms that confer enhanced genotypic PUE. Genes identified in such studies may prove useful in breeding programs but may also provide targets for genetic manipulation in addition to the well-known genes that are affected by P-deficiency stress.

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6. Conclusions and Future Prospective 6.1. PAE versus PUE—Does one offer better chances of success? Breeding P-efficient crop cultivars and developing more P-efficient agronomic practices are needed for future food security and environmental protection because the current global P cycle is not sustainable (Cordell et al., 2009). Breeding efforts in the past have disproportionally focused on improving PAE of crops (Wissuwa et al., 2009), and while there is no doubt about the importance of developing cultivars that are more efficient at acquiring soil P, it is equally obvious that improving the PUE of crop cultivars would complement PAE traits in an ideal fashion. Despite this, we are not aware of any serious effort to specifically improve PUE in plant breeding. This is to some extent due to the difficulty in evaluating PUE without having genotypic rankings confounded by differences in HI and P uptake. A second reason may have been that genotypic variation for PAE typically appears to be higher than for PUE (Parentoni and Ju´nior, 2008; Wissuwa and Ae, 2001). However, upon closer inspection of the data, this assessment no longer holds because values typically shown for P uptake (or P content) do not represent measurements of the uptake process itself but rather their aggregate effect (Wissuwa et al., 2005) over extended periods up to an entire crop cycle. If two genotypes differ twofold in P uptake after a 100-day growth period, this does not mean that they differ by an equally large margin for the causal mechanisms that trigger more efficient P uptake. Genotypic differences in causal mechanisms can be rather small (Wissuwa, 2003) and differences in P uptake may even be caused by changes in PUE (Fig. 3), particularly by root morphological adaptations that reduce the cost of producing and maintaining roots (Lynch and Ho, 2005). Thus, while data from screening experiments certainly overestimate the genotypic variation present for mechanisms enhancing PAE, the full benefits of increased PUE are likely underestimated. Further, due to the impact of P uptake on PUE and vice versa, determining the relative contributions of PUE and PAE to P efficiency may not be possible.

6.2. Screening methods, targets, and possible results PAE has an overriding and unavoidable influence on PUE rankings in soilbased screening experiments, and this has led to confounded results and misleading conclusions in a variety of studies on PUE (Rose et al., 2011). One would therefore ideally screen at equal P uptake or derive genotypespecific P response curves over a target range of P content (Rose et al., 2011). While the latter option would be ideal, the effort needed to produce response curves for a large number of genotypes would in most cases be

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prohibitive. We therefore tested of a modified nutrient solution screening technique that uncouples PAE and PUE by ensuring that all screened genotypes have the same P uptake. Results showed that genotypic differences in PUE do exist in the absence of differences in P uptake (Rose et al., 2011), that genotypic rankings of the unbiased screening method differed considerable from those in conventional soil-based method, and that rankings for PUE in shoot and root tissue were not related. While further confirmation is needed to establish that the genetic basis of PUE differs from shoot to root tissue, such a notion makes intuitive sense since shoots and roots perform entirely different functions. PUE mechanisms could therefore relate to different physiological processes or morphological attributes. The tissue specificity of PUE does become more obvious if PUE was defined in a more root-specific way as root surface area (rather than biomass) per milligram P, since root-specific morphological modifications (root hairs, aerenchyma, proportion of vascular tissue) could be targeted with the aim of producing a low-cost root system (Lynch and Ho, 2005). Yet another target for improvements in PUE is the grain tissue. Since P concentrations in grains tend to be an order of magnitude higher compared to roots or shoots (Rose et al., 2010), and theoretically higher than needed for normal physiological function (Raboy, 2009), it is likely that some P translocation and loading mechanisms would determine grain PUE, rather than physiological redistribution or substitution mechanisms expected to operate in shoot or root tissue. Although QTL for grain P concentration have been identified (Stangoulis et al., 2007; Zhao et al., 2008), such QTL may be related to either yield formation (causing a dilution effect on grain P concentration; Batten, 1992) or plant P uptake, which determines the available pool of P that can be remobilized to developing grains. Another critical question is what are the minimum P requirements of developing seeds for maximum yield formation and subsequent germination of seeds? These issues, and the more fundamental question of which phosphate transporters are involved in loading P into grains and how are they regulated at the molecular level, are critical areas of research that need to be addressed. However, while this remains an exciting emerging area of research from a plant physiological and P-efficiency point of view, the potential impact of a low-grain-P trait on human health and seedling vigor cannot be ignored. Further research is needed to address these concerns, but such research cannot be adequately conducted until either low-grain-P near isogenic lines or mutants become available.

6.3. Marker-assisted selection—A paradigm shift in breeding suited for PUE Traditional plant breeding relied almost entirely on phenotypic selection, with grain yield being the far most important selection criterion. Selecting for tissue-specific PUE would have had little appeal for breeders, given that

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a direct positive effect of PUE on grain yield is difficult to prove considering that factors like HI or PAE tend to obscure effects of higher PUE. The recent paradigm shift in plant breeding toward marker-assisted selection (MAS) now allows for the introgression of traits that are difficult to evaluate and, further, assures that any undesirable attributes of a donor variety are efficiently eliminated (Septiningsih et al., 2009). The yield potential of the donor parent is therefore of little consequence in MAS, which now enables breeders to make full use of the genetic variation present in genebank collections. The task at hand therefore is to evaluate a large number of genebank accessions for specific PUE traits and to identify loci controlling these traits. Genome-wide association mapping, where marker information of genebank accessions is used in conjunction with some phenotypic data to identify loci associated with the phenotype, is ideally suited to identify loci controlling PUE in various tissues. Once superior alleles for such traits have been identified, they can be transferred via MAS to a recipient variety with high yield potential. Since this process is highly efficient, it is feasible to combine (pyramid) the most promising PUE loci with loci for high PAE in a single recipient variety, thus creating a variety with superior overall P efficiency.

6.4. Remaining questions As plants suffer higher levels of P-deficiency stress, their PUE increases. It is therefore tempting to speculate that alleles conferring higher PUE will be most useful under strongly P-limiting conditions and that screening should also take place under these conditions. While such conditions are common where farmers have no access to P fertilizers or are too resource-poor to “invest” in fertilizer application (Ismail et al., 2007), in reality the majority of crops experiencing P deficiency only suffer a mild form, and estimating potential benefits of enhanced PUE under such mild P deficiency is much less straightforward. Moreover, the utility of high-PUE traits identified in strongly Plimiting conditions for improving PUE in plants suffering milder P-deficiency stress is not known. A further critical question is whether genotypes (or QTL/ genes) identified in artificial screening methods that separate P uptake and PUE ultimately enhance P efficiency under field conditions. Improving root/shoot PUE in high-input or P-replete conditions would also be desirable, but we believe this cannot be achieved through plant improvement. Data presented in Table 4d indicated a very tight negative correlation between PUE and P uptake under high-P input, which essentially means that one would have to select against P uptake in order to improve PUE. That would be counterproductive as fertilizer P would remain in soil unused. Thus, in high-input systems, what should be targeted is the overall system P efficiency and reductions in P fertilizer application, possibly in combination with improved fertilizer timing or

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placement, appear most suitable. Targeting grain PUE may be of additional benefit because more P will be retained on-farm if the straw is not exported from fields. Much effort in breeding P-efficient crops has focused on improving PAE because many resource-poor farmers cannot afford P fertilizers and even when P fertilizers are used they become gradually immobilized in soils over time (Richardson et al., 2011). The downside of focusing solely on improving PAE is that such genotypes increase the rate of mining of soil P by removing more P in harvested products (Henry et al., 2010) and little of the P removed in harvested products is recycled back onto fields (Cordell et al., 2009). While much remains unknown about mechanisms that could enhance PUE beyond the level already present in most crops, and whether they can be exploited in breeding, research to address the gaps is warranted: if plant breeding is to contribute to mitigating an unsustainable global P cycle, then high-PUE traits must ultimately complement high PAE traits in crop cultivars.

REFERENCES Adu-Gyamfi, J. J., Fujita, K., and Ogata, S. (1989). Phosphorus absorption and utilization efficiency of pigeon pea (Cajanus cajan (L) Millsp.) in relation to dry matter production and dinitrogen fixation. Plant Soil 119, 315–324. Ahmad, Z., Gill, M. A., and Qureshi, R. H. (2001). Genotypic variations of phosphorus utilization efficiency of crops. J. Plant Nutrition 24, 1149–1171. Akhtar, M. S., Oki, Y., and Adachi, T. (2008). Genetic variability in phosphorus acquisition and utilization efficiency from sparingly soluble P-sources by Brassica cultivars under P-stress environment. J. Agron. Crop Sci. 194, 380–392. Akhtar, M. S., Oki, Y., and Adachi, T. (2009). Mobilization and acquisition of sparingly soluble P-sources by Brassica cultivars under P-starved environment I. Differential growth response, P-efficiency characteristics and P-remobilization. J. Integr. Plant Biol. 51, 1008–1023. Arau´jo, A. P., Teixeira, M. G., and De Almeida, D. L. (1997). Phosphorus efficiency of wild and cultivated genotypes of common bean (Phaseolus vulgaris L.) under biological nitrogen fixation. Soil Biol. Biochem. 29, 951–957. Aziz, T., Gill, M. A., Rahmatullah, M. A., and Mansoor, T. (2005). Differences in phosphorus absorption, transport and utilization by twenty rice (Oryza saliva L.) cultivars. Pak. J. Agric. Sci. 42, 8–15. Aziz, T., Rahmatullah, M. A., Tahir, M. A., Ahmad, I., and Cheema, M. A. (2006). Phosphorus utilization by six Brassica cultivars (Brassica juncea L.) from tri-calcium phosphate; a relatively insoluble compound. Pak. J. Bot. 38, 1529–1538. Batjes, N. H. (1997). A world data set of derived soil properties by FAO-UNESCO soil unit for global modeling. Soil Use Manag. 13, 9–16. Batten, G. D. (1986). The uptake and utilization of phosphorus and nitrogen by diploid, tetraploid and hexaploid wheats (Triticum spp.). Ann. Bot. 58, 49–59. Batten, G. D. (1992). A review of phosphorus efficiency in wheat. Plant Soil 146, 163–168. Batten, G. D., and Khan, M. A. (1987). Uptake and utilisation of phosphorus and nitrogen by bread wheats grown under natural rainfall. Aust. J. Exp. Agric. 27, 405–410.

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