Quantitative Trait Loci, Epigenetics, Sugars, and Micrornas: Quaternaries in Phosphate Acquisition and Use
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Future Perspectives in Plant Biology Quantitative Trait Loci, Epigenetics, Sugars, and MicroRNAs: Quaternaries in Phosphate Acquisition and Use Carroll P. Vance* United States Department of Agriculture/Agricultural Research Service, Plant Science Research Unit, Agronomy and Plant Genetics Department, University of Minnesota, St. Paul, Minnesota 55108 Phosphorus (P) is a critical element for plant growth the tropics and subtropics are particularly prone to P and is frequently the limiting nutrient in many soils. deficiency. Continued production and application of P fertilizer Mined rock phosphate, a nonrenewable resource, is relies on a nonrenewable resource that will peak in the primary source of P fertilizer (Steen, 1998; Tiessen, about 2050. This will result in significantly increased 2008; Cordell et al., 2009). Easily mined, high-quality cost, particularly for developing countries. Significant rock phosphate sources are projected to be depleted research efforts in the genomics of P stress have shown within 30 to 50 years. In addition, the world’s major that many suites of genes regulated in a coordinated reserves of rock phosphate are located in Morocco and fashion are involved in plant acclimation to P defi- China. Uncertain political issues could limit access to ciency. These genomic studies, in conjunction with tra- the world’s P resources. Coalescence of these factors ditional plant breeding, have shown that P-acclimation as well as production of food for energy has seen traits are controlled by multiple genes, most probably P-fertilizer costs increase 6- to 9-fold in the past few in quantitative trait loci (QTLs). Future development years. A potential phosphate crisis looms for agricul- of near isogenic lines (NILs) and recombinant inbred ture in the 21st century (Abelson, 1999; Tiessen, 2008). lines (RILs) coupled to next-generation sequencing Application of P fertilizer, however, is problematic will facilitate the cloning of genes in QTLs regulating for both the intensive and extensive agriculture of the P-deficiency acclimation. Defining the role of epigenetic developed and developing worlds, respectively. Un- regulation of gene expression in adaptation to abiotic der adequate P fertilization, only 20% or less of that stress will provide new targets for improving plant applied is removed in the first year’s growth. This adaptation to P starvation. Cross talk between sugars, results in P loading of prime agricultural land and microRNAs (miRNAs), and P-starvation-induced gene increased P runoff (Kirkby and Johnston, 2008; White expression may be significant to understanding the and Hammond, 2008). An even greater concern is the fundamental underpinning of plant adaptation to nu- lack of available P fertilizers for extensive agriculture trient stresses. Plants with highly efficient P acquisition in the tropics and subtropics, where the majority of and use could reduce the need for P fertilizer in the Earth’s people live. Lack of infrastructure, money, and developed world, thereby ameliorating the overuse of P transportation make P fertilization unattainable for while concurrently enhancing yield in the developing these areas. It is imperative that within the next 40 world, where P is frequently unavailable. years plant biologists understand the genetic basis for acclimation to P deficiency and through traditional selection and/or biotechnology develop germplasm sources with improved P-use efficiency. IMPORTANCE OF P Plant responses to P-stress conditions involve changes in both shoot and root development (Lynch, P is one of 17 essential elements (nutrients) required 1995; Lynch and Brown, 2001; Lo´pez-Bucio et al., 2003; for plant growth (Tiessen, 2008; Cordell et al., 2009). Bucciarelli et al., 2006; Lambers et al., 2006; Herna´ndez The P concentration in plants ranges from 0.05% to et al., 2007). P-deficient plants display (1) delayed leaf 0.50% dry weight. The concentration gradient from the development and reduced photosynthetic capacity, (2) soil solution P to plant cells exceeds 2,000-fold, with an m reduced axillary shoot emergence and elongation average free P of 1 to 5 M in the soil solution (Bieleski, (stunted plants), (3) impaired flower development, 1973; Schachtman et al., 1998). Although bound P is (4) increased anthocyanin accumulation, (5) increased quite abundant in many soils, it is largely unavailable root-shoot ratio, (6) altered root architecture, and (7) for uptake, and P is frequently the most limiting increased exudation from roots of organic acids, phe- element for plant growth and development (Tiessen, nolics, protons, and enzymes. 2008; Cordell et al., 2009). The acid-weathered soils of Because roots are the primary site for acquiring P, they have become a rich topic for developmental and * E-mail [email protected]. genetic studies. Soil P limitation is a primary effector www.plantphysiol.org/cgi/doi/10.1104/pp.110.161067 of root architecture (Dinkelaker et al., 1995; Williamson Ò 582 Plant Physiology , October 2010, Vol. 154, pp. 582–588, www.plantphysiol.org Ó 2010 American Society of Plant Biologists Plant Phosphorus Stress et al., 2001; Lo´pez-Bucio et al., 2003; Lambers et al., et al., 2006), soybean (Glycine max; Li et al., 2005; 2006) and is known to impact all aspects of root growth Zhang et al., 2009), barley (Hordeum vulgare; Gahoonia and development. Phenotypic and genotypic adapta- and Nielsen, 2004), and maize (Zea mays; Zhu et al., tions to P deficiency involve changes in root architec- 2005; Chen et al., 2009; Hochholdinger and Tuberosa, ture that facilitate the acquisition of P from the topsoil. 2009). Adaptations that enhance acquisition of P from topsoil Utilizing a mapping population derived from a are important because of the relative immobility of P cross of the intolerant ‘Nipponbare’ cultivar with the in soil, with the highest concentrations usually found tolerant landrace ‘Kasalath,’ Wissuwa et al. (2002) in the topsoil. Lynch and Brown (2001) refer to identified a QTL for tolerance to low P in rice desig- P-deficiency-induced modifications of root architecture nated Phosphorus uptake1 (Pup1). Introgression of as adaptations for topsoil foraging. Root characteris- Pup1 into NILs allowed fine mapping of the Pup1 tics associated with improved topsoil foraging for locus to the long arm of chromosome 12 (15.31–15.47 scarce P are a more shallow horizontal basal root Mb) on the basis of the Nipponbare reference genome growth angle, increased adventitious root formation, (Heuer et al., 2009). Next-generation sequencing was enhanced lateral root proliferation, and increased root used to characterize the genomic (278 kb) introgres- hair density and length. The phenotypic complexity of sion region. Although the gene(s) regulating the Pup1 plant acclimation to P deficiency reflects the polygenic phenotype has yet to be identified, it is worthwhile to nature of these processes. note that the Pup1 region is found in 50% of the rice In recent years, significant inroads into understand- accessions adapted to stress-prone environments (Chin ing biochemical and molecular events involved in et al., 2010). plant acclimation to P stress have been made through In common bean, RILs were developed for shallow- comparative microarray and macroarray studies of rooted and deep-rooted phenotypes (Rubio et al., P-deficient plants as compared with P-sufficient plants. 2003). Under field conditions, when available P was In addition, definition of single-gene mutants in Arab- concentrated in the topsoil layer, the shallow-rooted idopsis (Arabidopsis thaliana) that show impaired P RILs were more productive and had a competitive signaling has demonstrated the role of transcription advantage over deep-rooted RILs. Further analysis of factors involved in P-induced gene expression. The the RILs by Liao et al. (2004) showed 16 QTLs control- importance of miR399 in P signal transduction has also ling the root traits. Adventitious root formation in 84 been a fruitful avenue of research. In coming years, RILs grown under limiting P conditions was shown to complementary research approaches that utilize next- be important for P acquisition in common bean (Ochoa generation sequencing coupled to analysis of well- et al., 2006). The QTLs for root traits related to low P defined plant germplasm containing QTLs for enhanced tolerance were mainly located on linkage groups B2 P-stress tolerance will lead to the identity of genome and B9. One QTL on linkage group B9 accounted for regulatory elements. Moreover, plants exposed to biotic 61% of the total phenotypic variation. Beebe et al. stress, such as diseases, undergo epigenetic changes (2006) evaluated 71 RILs grown under either low P or leading to resistance responses, but the importance of high P and identified 26 QTLs affecting P accumula- epigenetic mechanisms in adaptation to abiotic stress is tion and root architecture. Enhanced P uptake was an underdeveloped discipline. Lastly, while sugars can associated with basal root development. Development act as signal molecules in several developmental re- of NILs of common bean having enhanced P tolerance sponses and have been implicated in P-stress responses, and shallow basal roots will provide the germplasm it is unclear how sugars moderate the transcriptional resources for further fine mapping of important traits. regulation of gene expression. This contribution will The common bean genome is currently being se- address the implications of next-generation sequencing, quenced. Having a reference genome and NIL genetic QTLs, epigenetics, and sugar-miRNA cross talk in plant resources for common bean coupled with next-generation acclimation to P deficiency. high-throughput RNA sequencing (RNA-seq) will fa- cilitate fine mapping and candidate gene(s) identifica- tion regulating P tolerance and root traits in common bean. QTLS ASSOCIATED WITH P-STRESS TOLERANCE AND ACCLIMATION Tuberosa and Salvi (2007) developed a library of maize introgressed lines from B73 (recurrent parent) Genetic variability for the complex root and shoot crossed with Gaspe Flint (donor parent) to identify responses to P-limiting conditions has been demon- major QTLs for root architecture and growth that map strated for a wide range of species.