Quantitative Trait Loci for Root Architecture Traits Correlated with Phosphorus Acquisition in Common Bean

Low soil P availability is a primary constraint to common bean (Phaseolus vulgaris L.) production in Latin America and Africa. Substantial genotypic variation in bean adaptation to low phosphorus (LP) availability has been linked with root traits that enhance the efficiency of soil foraging. The objectives of this study were to identify quantitative trait loci (QTLs) for P accumulation and associated root architectural traits, to facilitate genetic improvement and to reveal physiological relationships. Eighty-six F5.7 recombinant inbred lines (RILs) were developed from a cross between G19833, an Andean landrace with high total P accumulation, and DOR 364, a Mesoamerican cultivar with low total P accumulation in LP conditions. A genetic map constructed with restriction fragment length polymorphisms (RFLPs), microsatellites, and PCR-based markers covering 1703 centimorgans (cM) total genetic distance and all eleven linkage groups (LGs) was used for QTL analysis. Seventy-one RILs were evaluated in the field at high phosphorus (HP) and LP for P accumulation, total root length (RL), specific RL, and plant dry weight (DW), while all 86 RILs were evaluated in a hydroponic system in the greenhouse for tap, basal, total, and specific RL and plant DW. Phosphorus accumulation in the field correlated with root parameters measured in the greenhouse. A total of 26 individual QTLs were identified for P accumulation and associated root characters using composite interval mapping (CIM) analysis. Phosphorus accumulation QTLs often coincided with those for basal root development, thus, basal roots appear to be important in P acquisition. Independent QTLs were identified for basal and taproot development, and for specific RL. Distinct QTLs for greater specific RL had positive, null and negative effects on P accumulation. Our results confirm the importance of root structure for LP adaptation and highlight the need for a more detailed understanding of root architectural traits for phenotypic as well as marker-aided selection of more P-efficient crops. PHOSPHORUS DEFICIENCY is a widespread nutrient constraint to crop production on tropical and subtropical soils that impacts millions of farmers, especially small landholders, on an area estimated at more than two billion hectares (Lynch, 1995, Fairhust et al., 1999). Correcting soil P deficiency with large applications of P fertilizer is not a viable option for most farmers in developing countries, and the inexpensive rock phosphate reserves remaining in the world could be depleted in as little as 60 to 80 yr. Therefore, sustainable P management in agriculture requires that researchers, plant breeders, and agronomists develop crops with enhanced P efficiency and management schemes that increase soil P availability (Vance, 2001). The ability of a plant to access available P under LP conditions depends on its RL and on several other morphological and physiological properties of the root (Raghothama, 1999), including association with arbuscular-mycorrhizal fungi that increase the soil volume from which P can be acquired (Marschner, 1995, p. 889) and root-induced changes in the rhizosphere such as P mobilization by root exudates (Gaume et al., 2001). Superior P acquisition, often referred to as phosphorusacquisition efficiency, differs from phosphorus-use efficiency, which is the plant’s ability to produce yield per unit of acquired P from soil (Lynch and Beebe, 1995; Rao et al., 1999). Understanding the mechanisms and genetic control of phosphorus acquisition and use efficiency and other aspects of LP tolerance would facilitate genetic improvement (Lynch and Beebe, 1995; Rao, 2001). Root architectural traits that enhance topsoil foraging appear to be particularly important for P acquisition efficiency and genotypic adaptation of common bean to LP soils (Lynch and Brown, 1999, 2001). Phosphorus availability regulates many features of root architecture, including adventitious rooting, aerenchyma formation, basal root elongation, basal root-growth angle, lateral rooting, root hair density, and root hair length (Bates and Lynch, 1996; Bonser et al., 1996; Borch et al., 1999; Fan et al., 2003; Liao et al., 2001; Ma et al., 2001a; Miller et al., 2003). These changes appear to act synergistically to enhance P acquisition, by enhancing the quality and quantity of soil foraging, and by reducing the metabolic costs of soil exploration (Lynch and Ho, 2004; Lynch and Brown, 2001; Ma et al., 2001b). Another trait that varies with P supply is specific RL, defined as length of root per unit root weight (Miller et al., 2003). Specific RL is related to root diameter (Fitter, 1985; Eissenstat 1992) and root tissue density (Fan et al., 2003; Ryser, 1996), and is important in determining the metabolic cost of root elongation, an important aspect of efficient soil exploration (Lynch and Ho, 2004). Specific RL varies among species and cultivars (de Willigen and van Noordwijk, S.E. Beebe, M. Rojas-Pierce, M.W. Blair, F. Muñoz, and J. Tohme, Centro Internacional de Agricultura Tropical (CIAT), A.A. 6713, Cali, Colombia; X. Yan, South China Agricultural Univ., Guangzhou, PRC; F. Pedraza, Univ. of Nebraska, Lincoln, NE, USA; F. Muñoz, Univ. of Florida, Hastings, FL, USA; J.P. Lynch, Pennsylvania State Univ., University Park, PA, USA. Received 15 Mar. 2005. *Corresponding author ([email protected]). Published in Crop Sci. 46:413–423 (2006). Genomics, Molecular Genetics & Biotechnology doi:10.2135/cropsci2005.0226 a Crop Science Society of America 677 S. Segoe Rd., Madison, WI 53711 USA Abbreviations: AFLP, amplified fragment length polymorphism; CIM, composite interval mapping; cM, centimorgan; DW, dry weight; HP, high phosphorus; LG, linkage group; LOD, base 10 algorithm of the likelihood ratio; LP, low phosphorus; QTL, quantitative trait locus; R, proportion of variance explained by QTL at test site; RL, root length; SCAR, sequence characterized amplified region; RAPD, randomly amplified polymorphic DNA; RFLP, restriction fragment length polymorphism; RIL, recombinant inbred line; TR, proportion of variance explained for the QTL and the background markers; TSP, triple super phosphate. R e p ro d u c e d fr o m C ro p S c ie n c e . P u b lis h e d b y C ro p S c ie n c e S o c ie ty o f A m e ri c a . A ll c o p y ri g h ts re s e rv e d . 413 Published online January 24, 2006