Root Phenes for Enhanced Soil Exploration and Phosphorus Acquisition: Tools for Future Crops

Abstract

Plant growth in the vast majority of terrestrial ecosystems is limited by low phosphorus availability. Over 70% of all terrestrial biomass occurs in low-phosphorus soils, including over half of agricultural land (Fig. 1). Phosphorus availability is declining in many systems because of soil degradation, which has affected over half of global agricultural land and 75% of agricultural land in Africa. Intensive phosphorus fertilization is uncommon in the low-input agriculture common in poor nations and has limitations as a long-term strategy because of limited reserves of high-grade phosphate ore deposits, the energy costs of producing fertilizer, and the environmental cost associated with intensive fertilization. The development of crops with greater phosphorus efficiency, defined as the ability to grow and yield in soils with reduced phosphorus availability, would substantially improve food security in developing nations, while enhancing the sustainability of agriculture in rich nations (Lynch, 2007). Map of global soil phosphorus availability. The dominance of red and light-gray colors, indicating suboptimal phosphorus availability for the growth of many plant species, indicates the importance of phosphorus availability as a primary limitation to plant productivity in terrestrial environments (from Jaramillo-Velastagui, 2011). Phosphate is highly immobile in soil, because it reacts with many chemical and biological soil constituents. Plant strategies to acquire phosphorus are therefore oriented around two basic themes: (1) soil exploration and (2) mobilization of phosphate from poorly available phosphorus pools in the rhizosphere. This Update focuses on phenes controlling soil exploration by roots, since they are subject to selection in crop breeding programs, and since root deployment is senior to many other root phenes affecting phosphorus acquisition, by determining the placement of root exudates and symbionts in specific soil domains, and thereby their functional benefit. Because of the immobility of phosphorus in soil, surface soil strata, enriched by the deposition of plant residues over time, generally have greater phosphorus availability than subsoil strata. Root traits that enhance topsoil foraging are therefore important for phosphorus acquisition. Substantial differences exist in topsoil foraging within and among species. Architectural traits associated with enhanced topsoil foraging include shallower growth angles of axial roots, enhanced adventitious rooting, a greater number of axial roots, and greater dispersion of lateral roots (Fig. 2). Root phenes associated with genotypic differences in adaptation to low phosphorus (from Lynch, 2007). In maize (Zea mays), bean (Phaseolus vulgaris), and soybean (Glycine max), shallower root growth angles (RGAs) of axial roots (basal roots in legumes, seminal and crown roots in maize; Fig. 3) increase topsoil foraging and thereby phosphorus acquisition. To determine the value of genotypic variation in RGA for phosphorus acquisition, it is useful to compare plants that have varying RGA but have otherwise similar phenotypes. Since RGA is controlled by multiple genes, useful tools for this analysis are recombinant inbred lines (RILs), created by repeated selfing of F2 progeny from parents contrasting for the phene of interest, resulting in a set of typically 100 or 200 homozygous inbred lines segregating for RGA yet sharing the same genetic background. RILs are powerful tools for the analysis of quantitative phenes like RGA since they permit the evaluation of a phene in an array of related yet distinct genomes. RILs are also useful for identifying genetic loci associated with phene expression (quantitative trait loci [QTL]). Cosegregation of QTL controlling a phene with phosphorus acquisition is strong evidence that the phene is important for phosphorus acquisition in a range of phenotypes. Analysis of maize and bean RILs varying in RGA shows that this phene has a dominant influence on phosphorus acquisition, accounting for up to 6-fold variation in phosphorus acquisition and 3-fold variation in yield of bean in low-phosphorus soil (Lynch and Brown, 2001), and 2-fold variation in phosphorus acquisition in maize (Zhu et al., 2005b). QTL associated with RGA in bean cosegregate with yield under phosphorus stress (Liao et al., 2004). Functional-structural modeling supports a positive role for RGA in phosphorus acquisition, showing that in stratified soils shallow RGA increases phosphorus acquisition by increasing topsoil foraging, and that in soils with uniform phosphorus distribution shallow RGA improves phosphorus acquisition by reducing competition for phosphorus among roots of the same plant (Lynch and Brown, 2001). RGA of axial roots is an important phene for topsoil foraging and phosphorus acquisition in annual crops. Shallow versus deep basal RGAs in two common bean genotypes grown in the field in South Africa. The main structural roots of annual legumes are