Terry J. Rose

Enhancing phosphorus and zinc acquisition efficiency in rice: a critical review of root traits and their potential utility in rice breeding

Background Rice is the worlds most important cereal crop and phosphorus (P) and zinc (Zn) deficiency are major constraints to its production. Where fertilizer is applied to overcome these nutritional constraints it comes at substantial cost to farmers and the efficiency of fertilizer use is low. Breeding crops that are efficient at acquiring P and Zn from native soil reserves or fertilizer sources has been advocated as a cost-effective solution, but would benefit from knowledge of genes and mechanisms that confer enhanced uptake of these nutrients by roots. Scope This review discusses root traits that have been linked to P and Zn uptake in rice, including traits that increase mobilization of P/Zn from soils, increase the volume of soil explored by roots or root surface area to recapture solubilized nutrients, enhance the rate of P/Zn uptake across the root membrane, and whole-plant traits that affect root growth and nutrient capture. In particular, this review focuses on the potential for these traits to be exploited through breeding programmes to produce nutrient-efficient crop cultivars. Conclusions Few root traits have so far been used successfully in plant breeding for enhanced P and Zn uptake in rice or any other crop. Insufficient genotypic variation for traits or the failure to enhance nutrient uptake under realistic field conditions are likely reasons for the limited success. More emphasis is needed on field studies in mapping populations or association panels to identify those traits and underlying genes that are able to enhance nutrient acquisition beyond the level already present in most cultivars.

Rethinking Internal Phosphorus Utilization Efficiency: A New Approach Is Needed to Improve PUE in Grain Crops

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.

Response to zinc deficiency of two rice lines with contrasting tolerance is determined by root growth maintenance and organic acid exudation rates, and not by zinc-transporter activity

*Zinc (Zn)-deficient soils constrain rice (Oryza sativa) production and cause Zn malnutrition. The identification of Zn-deficiency-tolerant rice lines indicates that breeding might overcome these constraints. Here, we seek to identify processes underlying Zn-deficiency tolerance in rice at the physiological and transcriptional levels. *A Zn-deficiency-tolerant line RIL46 acquires Zn more efficiently and produces more biomass than its nontolerant maternal line (IR74) at low [Zn](ext) under field conditions. We tested if this was the result of increased expression of Zn(2+) transporters; increased root exudation of deoxymugineic acid (DMA) or low-molecular-weight organic acids (LMWOAs); and/or increased root production. Experiments were performed in field and controlled environment conditions. *There was little genotypic variation in transcript abundance of Zn-responsive root Zn(2+)-transporters between the RIL46 and IR74. However, root exudation of DMA and LMWOA was greater in RIL46, coinciding with increased root expression of putative ligand-efflux genes. Adventitious root production was maintained in RIL46 at low [Zn](ext), correlating with altered expression of root-specific auxin-responsive genes. *Zinc-deficiency tolerance in RIL46 is most likely the result of maintenance of root growth, increased efflux of Zn ligands, and increased uptake of Zn-ligand complexes at low [Zn](ext); these traits are potential breeding targets.

Wheat, canola and grain legume access to soil phosphorus fractions differs in soils with contrasting phosphorus dynamics

Despite the high phosphorus (P) mobilizing capacity of many legumes, recent studies have found that, at least in calcareous soils, wheat is also able to access insoluble P fractions through yet unknown mechanism(s). We hypothesized that insoluble P fractions may be more available to non-legume plants in alkaline soils due to increased dissolution of the dominant calcium(Ca)-P pool into depleted labile P pools, whereas non-legumes may have limited access to insoluble P fractions in iron(Fe)- and aluminium(Al)-P dominated acid soils. Four crop species (faba bean, chickpea, wheat and canola) were grown on two acid and one alkaline soil under glasshouse conditions to examine rhizosphere processes and soil P fractions accessed. While all species generally depleted the H2O-soluble inorganic P (water Pi) pool in all soils, there was no net depletion of the labile NaHCO3-extractable inorganic P fraction (NaHCO3 Pi) by any species in any soil. The NaOH-extractable P fraction (NaOH Pi) in the alkaline soil was the only non-labile Pi fraction depleted by all crops (particularly canola), possibly due to increases in rhizosphere pH. Chickpea mobilized the insoluble HCl Pi and residual P fractions; however, rhizosphere pH and carboxylate exudation could not fully explain all of the observed Pi depletion in each soil. All organic P fractions appeared highly recalcitrant, with the exception of some depletion of the NaHCO3 Po fraction by faba bean in the acid soils. Chickpea and faba bean did not show a higher capacity than wheat or canola to mobilize insoluble P pools across all soil types, and the availability of various P fractions to legume and non-legume crops differed in soils with contrasting P dynamics.

Stress Response Versus Stress Tolerance: A Transcriptome Analysis of Two Rice Lines Contrasting in Tolerance to Phosphorus Deficiency

Transcriptional profiling has identified genes associated with adaptive responses to phosphorus (P) deficiency; however, distinguishing stress response from tolerance has been difficult. We report gene expression patterns in two rice genotypes (Nipponbare and NIL6-4 which carries a major QTL for P deficiency tolerance (Pup1)) grown in soil with/without P fertilizer. We tested the hypotheses that tolerance of NIL6-4 is associated with (1) internal P remobilization/redistribution; (2) enhanced P solubilization and/or acquisition; and (3) root growth modifications that maximize P interception. Genes responding to P supply far exceeded those differing between genotypes. Genes associated with internal P remobilization/redistribution and soil P solubilization/uptake were stress responsive but often more so in intolerant Nipponbare. However, genes putatively associated with root cell wall loosening and root hair extension (xyloglucan endotransglycosylases/hydrolases and NAD(P)H-dependent oxidoreductase) showed higher expression in roots of tolerant NIL6-4. This was supported by phenotypic data showing higher root biomass and hair length in NIL6-4.

Rethinking Internal Phosphorus Utilization Efficiency

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.

Phospholipids in rice: Significance in grain quality and health benefits: A review

Phospholipids (PLs) are a major class of lipid in rice grain. Although PLs are only a minor nutrient compared to starch and protein, they may have both nutritional and functional significance. We have systemically reviewed the literature on the class, distribution and variation of PLs in rice, their relation to rice end-use quality and human health, as well as available methods for analytical profiling. Phosphatidylcholine (PC), phosphatidylethanolamine (PE), phosphatidylinositol (PI) and their lyso forms are the major PLs in rice. The deterioration of PC in rice bran during storage was considered as a trigger for the degradation of rice lipids with associated rancid flavour in paddy and brown rice. The lyso forms in rice endosperm represent the major starch lipid, and may form inclusion complexes with amylose, affecting the physicochemical properties and digestibility of starch, and hence its cooking and eating quality. Dietary PLs have a positive impact on several human diseases and reduce the side-effects of some drugs. As rice has long been consumed as a staple food in many Asian countries, rice PLs may have significant health benefits for those populations. Rice PLs may be influenced both by genetic (G) and environmental (E) factors, and resolving G×E interactions may allow future exploitation of PL composition and content, thus boosting rice eating quality and health benefits for consumers. We have identified and summarised the different methods used for rice PL analysis, and discussed the consequences of variation in reported PL values due to inconsistencies between methods. This review enhances the understanding of the nature and importance of PLs in rice and outlines potential approaches for manipulating PLs to improve the quality of rice grain and other cereals.

The effectiveness of deep placement of fertilisers is determined by crop species and edaphic conditions in Mediterranean-type environments: a review

Much of our knowledge of plant growth in response to soil nutrient supply comes from studies under homogeneous soil conditions. However, the adoption of reduced or nil tillage and shallow banding of fertilisers at the time of seeding causes spatially variable distribution and availability of soil nutrients in agricultural lands. Soil available nutrients, particularly the poorly mobile ones such as phosphorus (P), potassium (K), zinc (Zn), manganese (Mn), and copper (Cu), stratify within the fertilised topsoil. In water-limited environments where the topsoil is prone to drying, soil nutrient stratification may influence nutrient availability and plant uptake because of impeded root growth or reduced diffusion of immobile nutrients to the root surface, or more likely a combination of both factors. Placing fertilisers deeper in the soil profile could increase nutrient acquisition and utilisation by plants as fertiliser nutrients are in the moist soil for a longer part of the growing season. However, the effectiveness of deep placement of fertilisers may also be determined by soil texture, tillage, fertilising history, nutrient mobility, and crop species. In Mediterranean-type climates of southern Australia, a yield response of winter crops to deep fertiliser mostly occurs on infertile sandy soils in low rainfall regions. This contrasts with the responses of winter and summer crops in northern Australia on soils with optimum-to-high nutrients but subjected to rapid and frequent drying of topsoil because of high temperatures and high evaporation demand during the growing season. The pattern of nutrient accumulation by crop species (indeterminate v. determinate) and the mobility of mineral nutrients in the phloem would also modify the effectiveness of deep-placed nutrients under drought. The complexity of plant responses to subsoil nutrition may suggest that before adopting deep fertiliser practice in a paddock it is essential to understand the effects of edaphic and climatic conditions, soil management, and plant-soil interactions in order to achieve maximum yield benefit.

Improving phosphorus efficiency in cereal crops: Is breeding for reduced grain phosphorus concentration part of the solution?

Given the non-renewable nature of global phosphate reserves, there is a push to increase the phosphorus (P) efficiency of agricultural crops. Research has typically focussed on investigating P acquisition efficiency or internal P utilization efficiency to reduce crop fertilizer requirements. A novel option that would reduce the amount of P exported from fields at harvest, and may ultimately reduce P fertilizer requirements, would be to reduce the amount of P translocated to grains to minimize grain P concentrations. While such a trait has been mentioned in a number of studies over the years, there has not been a concerted effort to target this trait in breeding programs. In this perspective piece we explore the reasons why a low grain P trait has not been pursued, and discuss the potential benefits and drawbacks of such a trait in the context of breeding to improve the P efficiency of cropping systems.

Enhanced biological N2 fixation and yield of faba bean (Vicia faba L.) in an acid soil following biochar addition: dissection of causal mechanisms

Background and aimsAcid soils constrain legume growth and biochars have been shown to address these constraints and enhance biological N2 fixation in glasshouse studies. A dissection of causal mechanisms from multiple crop field studies is lacking.MethodsIn a sub-tropical field study, faba bean (Vicia faba L.) was cultivated in rotation with corn (Zea mays) following amendment of two contrasting biochars, compost and lime in a rhodic ferralsol. Key soil parameters and plant nutrient uptake were investigated alongside stable 15 N isotope methodologies to elucidate the causal mechanisms for enhanced biological N2 fixation and crop productivity.ResultsBiological N2 fixation was associated with plant Mo uptake, which was driven by reductions in soil acidity following lime and papermill (PM) biochar amendment. In contrast, crop yield was associated with plant P and B uptake, and amelioration of soil pH constraints. These were most effectively ameliorated by PM biochar as it addressed both pH constraints and low soil nutrient status.ConclusionsWhile liming resulted in the highest biological N2 fixation, biochars provided greater benefits to faba bean yield by addressing P nutrition and ameliorating Al toxicity.