The identification of an enzyme in rice that confers improved plant yields on phosphorus-deficient soils could open up new avenues for generating nutrient-efficient crops that can thrive on marginally fertile soils. See Letter p.535
Phosphorus is probably the most limiting mineral nutrient for plants. Many of our planet's soils are low in the mineral, and this includes approximately half of the world's agricultural lands1. Hence, there is considerable interest in developing plant varieties that are more phosphorus efficient — that is, crops that can produce higher yields while using less soil phosphorus. On page 535 of this issue, Gamuyao et al.2 report the identification of the first phosphorus-efficiency gene in plants. The gene encodes a protein kinase enzyme that significantly enhances grain yield from rice plants grown on phosphorus-deficient soils.
Multiple factors contribute to the phosphorus problem. A large fraction of soil phosphorus is held very tightly to the surface of soil particles or is tied up (fixed) as organic phosphorus compounds, and is therefore relatively unavailable for plant uptake (Fig. 1). Furthermore, many low-phosphorus regions are in developing countries, where soils are often degraded and where many farmers lack the financial resources to purchase phosphorus fertilizers. Thus, plant access to the mineral plays a part in the precarious food-security situation in some of these regions. To further exacerbate the problem, the phosphorus used in fertilizers is obtained from rock phosphate, which is a non-renewable resource that could be depleted in 50–100 years3. Even for the high-input agriculture common in developed countries, much of the fertilizer-derived phosphorus either becomes fixed (and therefore unavailable to plants) or is lost through leaching into ground and surface waters, which is damaging to the surrounding environment.
A possible way to circumvent these problems is to generate plant varieties that simply need less of the nutrient. This particular episode in that quest began around 15 years ago, when researchers from the group presenting the current paper began to study a subpopulation of rice plants called the aus varieties, which originated from nutrient-poor soils in India. There was a growing awareness that these traditional rice varieties were likely to be a rich source of genes encoding tolerance to abiotic stresses, such as prolonged flooding4. A genetic screen of multiple rice varieties led to the identification5 of Kasalath, an aus line that is significantly more phosphorus efficient than the varieties currently used for rice production. A subsequent genetic analysis of plants generated from a cross between Kasalath and a modern, phosphorus-inefficient rice variety determined that several regions of the rice genome are associated with improved phosphorus efficiency5,6. The phosphorus uptake (PUP) genomic region that has the largest effect is located on rice chromosome 12 and has been named Pup1 (ref. 7).
However, subsequent efforts to identify the specific gene, or genes, responsible for phosphorus efficiency in the Kasalath strain were complicated by the fact that greater phosphorus efficiency can arise from several aspects of plant physiology. For example, more-active root growth that positions roots closer to where the soil phosphorus is located, or greater root-mediated biological and chemical activity to solubilize and absorb fixed phosphorus can both lead to more efficient acquisition. In addition, more-efficient cellular use of the mineral can contribute to enhanced phosphorus efficiency.
To try to tease apart which of these processes are influenced by Pup1, the researchers used breeding techniques to introduce the Pup1-containing region into modern rice lines that are phosphorus inefficient. The offspring lines had significantly higher grain and biomass yields than the parent lines when grown on phosphorus-deficient soils, and physiological analysis showed that this resulted from significantly greater phosphorus uptake and accumulation8.
The research group subsequently compared9 the DNA sequence containing the Pup1 region in the Kasalath variety with the reference genome sequence for rice, which was generated from the modern variety, Nipponbare. The sequences differed considerably, with the Kasalath sequence containing several putative genes not present in Nipponbare. Gene-expression analysis allowed the authors to single out one of these inserted genes, which encodes a protein kinase. This gene is expressed at high levels in the roots of plants harbouring the Kasalath Pup1 region, and expression of the gene is further enhanced in phosphorus-deficient conditions.
In the current paper2, Gamuyao and colleagues further characterize this gene, which they have named PSTOL1, for phosphorus-starvation tolerance 1. The authors demonstrate that modern rice lines that are genetically engineered to overexpress PSTOL1 show significant increases in grain and biomass production compared with wild-type plants when the plants are grown on phosphorus-deficient soils. They also show that the PSTOL1 protein belongs to the receptor-like cytoplasmic kinase sub-group of protein kinases. This is interesting, because receptor-like kinases have been implicated in plant responses to several types of abiotic stress, including drought10.
By comparing the root architecture of rice plants overexpressing PSTOL1 with that of the corresponding lines lacking the kinase, the authors found that PSTOL1 expression resulted in increased early root growth and root proliferation, suggesting that the kinase enhances the plants' ability to 'mine' soil phosphorus. The proposal that PSTOL1 functions in root development and growth was supported by studies showing that PSTOL1 expression is confined to specific tissue regions where crown roots, which make up a substantial portion of the mature rice root system, begin to emerge.
These findings have opened up new avenues for improving crop plant phosphorus efficiency — and possibly the efficiency of the uptake of other nutrients as well. Considerable work remains to be done to elucidate the molecular mechanisms and downstream targets of PSTOL1. But the researchers are already attempting to translate their discoveries into improved phosphorus efficiency in rice crops by use of targeted inter-variety breeding. It will be interesting to see how stable this trait is in plant varieties from different genetic backgrounds and in different growth environments. In addition, the authors' earlier genetic screens identified other genomic regions associated with enhanced phosphorus efficiency, and it will be exciting to watch for the identification of specific genes within these regions, and for the discovery of potential synergistic effects on plant-nutrient efficiency when these genes or regions are combined. Finally, Gamuyao and colleagues' research has highlighted the value that lies in investigating traditional plant varieties for beneficial traits that might have been lost during domestication.
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Gamuyao, R. et al. Nature 488, 535–539 (2012).
Cordell, D., Drangert, J.-O. & White, S. Glob. Environ. Change 19, 292–305 (2009).
Xu, K. et al. Nature 442, 705–708 (2006).
Wissuwa, M. & Ae, N. Plant Breed. 120, 43–48 (2001).
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Wissuwa, M., Wegner, J., Ae, N. & Yano, M. Theor. Appl. Genet. 105, 890–897 (2002).
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