Phosphorus (P) is a critical element for plant growth and is frequently the limiting nutrient in many soils. Mined rock phosphate provides about 90% of the P fertilizer used for agriculture. Continued production and application of P fertilizer relies on this nonrenewable resource, for which availability may peak in about 2030. This will result in significantly increased cost, particularly for developing countries. The development of crop plants with more efficient P acquisition and use is a necessity for sustainable farming practices. Highly P-efficient plants could reduce the need for P fertilizer in the developed world, thereby ameliorating overuse of P, while concurrently enhancing yield in the developing world where P is frequently unavailable. Sustainable management of P in agriculture requires that plant biologists discover mechanisms that enhance P acquisition and exploit these adaptations to make plants more efficient at acquiring P, develop P-efficient germplasm, and advance crop management schemes that increase soil P availability. This special issue of Plant Physiology focuses on recent advances in understanding the genetics and biochemistry of plant P acquisition and use. Results obtained with both model and crop species demonstrate the complex genetic and developmental interactions involved in plant acclimation to P limitation. Below, we highlight some of the advances noted in this special issue.
Quantitative trait loci (QTLs) are typically regions of the genome associated with variation in the phenotype of interest. When recombinant inbred lines (RILs) and a reference genome are coupled to next generation sequencing, introgressed regions of the genome controlling traits of interest can be finely mapped, and potential gene candidates can be identified. The PUP1 locus in rice (Oryza sativa), which confers tolerance to P deficiency in soil, is currently the most promising QTL for development of P-tolerant rice varieties. Gene models based upon the PUP1 locus in the variety Kasalath were used to fine map a 278-kb QTL. Molecular markers, expression analyses, and partial allelic sequencing were tested in 80 diverse rice accessions. A core set of PUP1 markers was defined, and single nucleotide polymorphisms suitable for high-throughput genotyping were developed. Eight priority gene candidates were identified. The PUP1 locus was largely absent from irrigated rice varieties but was conserved in germplasm adapted to drought-prone environments. A marker-assisted backcrossing approach was used to introgress the PUP1 locus into five germplasm sources. Phenotypic evaluation of the introgression lines showed that incorporation of the PUP1 locus resulted in significantly enhanced grain yield in both rain-fed and irrigated environments under P deficiency conditions.
In comparison with phenotypic QTLs, expression QTLs (eQTLs) are regions of the genome associated with variation in gene expression related to traits of interest. Variation can arise because of sequence polymorphisms in target genes either in cis-regions (contiguous) or trans-regions (distal) of the genome. The analysis of eQTLs using RNA-seq or microarrays in conjunction with phenotypic QTLs in segregating lines offers great promise in defining the gene(s) controlling agronomically important growth and development traits. The eQTL architecture (regulatory hotspots) for plant adaptation to low P was determined in 78 RILs derived from a mapping population of Brassica rapa. Using microarrays, transcriptional profiles were determined in plants grown under optimal and low P conditions. Some 18,800 eQTLs were detected, with a notable trans-eQTL hotspot on chromosome A06. This hotspot was enriched for phosphate-responsive transcripts. A phosphate use efficiency QTL colocalized with the eQTL on chromosome A06. The genes located at hotspot on A06 contain potential targets for improving tolerance to low P.
Plant tolerance of P deficiency occurs through the expression of suites of genes leading to biochemical and developmental changes that facilitate acclimation to the stress. Previously, Suc has been implicated as playing an important role in phosphate deficiency-induced gene expression. Unequivocal support for the role of Suc in regulating phosphate deficiency gene expression is shown by defining the function of the hypersensitive to phosphate starvation1 (hps1) gene in Arabidopsis. The hsp1 mutant was identified in an Arabidopsis T-DNA activation library. The mutant showed greatly increased expression of acid phosphatases, increased anthocyanin, and more starch accumulation when grown under low phosphate conditions. The mutant phenotype of hsp1 appears to be because of overaccumulation of Suc in roots and shoots. Positional cloning of hsp1 revealed that the gene encodes SUC TRANSPORTER2 (SUC2). Further confirmation of the importance of Suc in P stress-induced gene expression was obtained by characterizing an Arabidopsis SUC2 null mutant. The SUC2 null mutant was severely impaired in root responses to low P. The genetic and genomic data present compelling evidence that Suc is a global regulator of plant responses to P starvation.
White lupin (Lupinus albus) is a legume that is very efficient at accessing poorly available P. It develops short, densely clustered tertiary lateral roots (cluster/proteoid roots) in response to P limitation. In this issue, two papers describe developmental and biochemical modifications that contribute to white lupin root acclimation to P stress. It is well established that under phosphate stress, plant membrane synthesis is redirected toward production of galacto/sulfo lipids to stabilize membranes as phospholipids are degraded for phosphate recycling. White lupin cluster roots have significantly enhanced expression of transcripts that annotate as glycerophosphodiesterase phosphodiesterase (GPXPDE). GPXPDE enzymes catalyze the hydrolysis of deacylated phospholipid glycerophosphodiesters to glycerol-3-phosphate and the corresponding alcohol. Enhanced expression of two white lupin GPXPDE genes (GPX PDE1 and GPX PDE2), and biochemical characterization of their corresponding proteins revealed that GPXPDE1 catalyzes cleavage of glycerophosphocholine, whereas GPXPDE2 shows highest activity with glycerophosphoinositol. The GPXPDE proteins were localized to the endoplasmic reticulum membrane of root hairs and epidermal cells. Silencing of either GPXPDE1 or GPXPDE2 impaired root hair development. An accompanying update reports on white lupin roots that were transformed with a white lupin cytokinin oxidase (CKX), a white lupin INDOLE ACETIC ACID7 (IAA7), or a Medicago truncatula CYTOKININ RECEPTOR (CRE), β-glucuronidase reporter promoter gene construct. Initial results show that CKX reporter activity appears reduced in P-deficient roots, whereas CRE and IAA7 reporter activity appears to be enhanced. The results support a role for the phosphate status of the plant in affecting the expression of genes involved in auxin and cytokinin signaling and cluster root development.
We hope that this Focus Issue will provide readers with insights into new research directions addressing plant acclimation to low P. Although research interest in plant acclimation to P stress has significantly expanded in recent years, and numerous reports have documented the molecular, biochemical, and developmental responses involved in plant tolerance, a clear strategy for improving phosphate acquisition and use is yet to be devised. Little is known about the role of epigenetics in regulating P stress gene expression. Only now are we coming to grips with the complexity of the genetic systems regulating plant adaptation to low P. Translation of fundamental knowledge about plant adaptation to low P into germplasm with improved P acquisition and use will require a marriage of genomics, plant biochemistry, and plant breeding disciplines. The further development of near inbred lines and RILs accompanied by next generation sequencing are imperative to identifying genes introgressed into QTLs that regulate plant tolerance to P starvation. Our goal for this Focus Issue is to provide students, postdoctoral associates, and educators with a framework for understanding plant response to low phosphate and to demonstrate the excitement generated through recent discoveries.