As an essential macroelement for all living cells, phosphorus is indispensable in agricultural production systems. Natural phosphorus reserves are limited, and it is therefore important to develop phosphorus-efficient crops. A major quantitative trait locus for phosphorus-deficiency tolerance, Pup1, was identified in the traditional aus-type rice variety Kasalath about a decade ago. However, its functional mechanism remained elusive until the locus was sequenced, showing the presence of a Pup1-specific protein kinase gene, which we have named phosphorus-starvation tolerance 1 (PSTOL1). This gene is absent from the rice reference genome and other phosphorus-starvation-intolerant modern varieties. Here we show that overexpression of PSTOL1 in such varieties significantly enhances grain yield in phosphorus-deficient soil. Further analyses show that PSTOL1 acts as an enhancer of early root growth, thereby enabling plants to acquire more phosphorus and other nutrients. The absence of PSTOL1 and other genes-for example, the submergence-tolerance gene SUB1A-from modern rice varieties underlines the importance of conserving and exploring traditional germplasm. Introgression of this quantitative trait locus into locally adapted rice varieties in Asia and Africa is expected to considerably enhance productivity under low phosphorus conditions.

BackgroundRice is the world's 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.ScopeThis 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.ConclusionsFew 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.

In rice, genotypic differences in phosphorus (P) uptake from P-deficient soils are generally proportional to differences in root biomass or surface area (RSA). It is not known to what extent genotypic variation for root efficiency (RE) exists or contributes to P uptake. We evaluated 196 rice accessions under P deficiency and detected wide variation for root biomass which was significantly associated with plant performance. However, at a given root size, up to 3-fold variation in total biomass existed, indicating that genotypes differed in how efficiently their root system acquired P to support overall plant growth. This was subsequently confirmed, identifying a traditional genotype, DJ123, with 2.5-fold higher RE (32.5 µg P cm(-2) RSA) compared with the popular modern cultivar IR64. A P depletion experiment indicated that RE could not be explained by P uptake kinetics since even IR64 depleted P to <20nM. A genome-wide association study identified loci associated with RE, and in most cases the more common marker type improved RE. This may indicate that modern rice cultivars lost the ability for efficient P uptake, possibly because they were selected under highly fertile conditions. One association detected on chromosome 11 that was present in a small group of seven accessions (including DJ123) improved RE above the level already present in many traditional rice accessions. This subspecies is known to harbor genes enhancing stress tolerance, and DJ123 may thus serve as a donor of RE traits and genes that modern cultivars seem to have lost.

Summary• 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-molecularweight 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 auxinresponsive 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.

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Depletion of non-renewable rock phosphate reserves and phosphorus (P) fertilizer price increases has renewed interest in breeding P-efficient varieties. Internal P utilization efficiency (PUE) is of prime interest because there has been no progress to date in breeding for high PUE. We characterized the genotypic variation for PUE present within the rice gene pool by using a hydroponic system that assured equal plant P uptake, followed by mapping of loci controlling PUE via Genome-Wide Association Studies (GWAS). Loci associated with PUE were mapped on chromosomes 1, 4, 11 and 12. The highest PUE was associated with a minor indica-specific haplotype on chromosome 1 and a rare aus-specific haplotype on chromosome 11. Comparative variant and expression analysis for genes contained within the chromosome 1 haplotype identified high priority candidate genes. Differences in coding regions and expression patterns between genotypes of contrasting haplotypes, suggested functional alterations for two predicted nucleic acid-interacting proteins that are likely causative for the observed differences in PUE. The loci reported here are the first identified for PUE in any crop that is not confounded by differential P uptake among genotypes. Importantly, modern rice varieties lacked haplotypes associated with superior PUE, and would thus benefit from targeted introgressions of these loci from traditional donors to improve plant growth in phosphorus-limited cropping systems.

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.

Despite the attention internal phosphorus utilization efficiency (PUE) of crops has received in the literature, little progress in breeding crop cultivars with high PUE has been made. Surprisingly few studies have specifically investigated PUE; instead, genotypic variation for PUE has been investigated in studies that concurrently assess phosphorus acquisition efficiency (PAE). We hypothesized that genotypic differences in PAE confound PUE rankings because genotypes with higher PAE suffer a lower degree of P stress, resulting in lower PUE. The hypothesis was tested by comparing soil-based screening to a modified technique whereby rice genotypes were grown in individual containers with a single dose of solution P, to eliminate differences in P uptake among genotypes. Genotypic differences in PUE were apparent in root and shoot tissue using the modified nutrient solution technique, but PUE rankings showed no correlation with those from traditional soil-based screening. We conclude that PUE in soil-based screening systems is unavoidably linked with genotypic PAE, resulting in PUE rankings confounded by differences in P uptake. Only screening techniques assuring equal P uptake are suitable for the exploitation of genotypic variation for PUE.