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A better understanding of the genetics of salinity tolerance in chickpea would enable breeding of salt tolerant varieties, offering potential to expand chickpea production to marginal, salinity-affected areas. A Recombinant Inbred Line population was developed using accelerated-Single Seed Descent of progeny from a cross between two chickpea varieties, Rupali (salt-sensitive) and Genesis836 (salt-tolerant). The population was screened for salinity tolerance using high-throughput image-based phenotyping in the glasshouse, in hydroponics, and across 2 years of field trials at Merredin, Western Australia. A genetic map was constructed from 628 unique in-silico DArT and SNP markers, spanning 963.5 cM. Markers linked to two flowering loci identified on linkage groups CaLG03 and CaLG05 were used as cofactors during genetic analysis to remove the confounding effects of flowering on salinity response. Forty-two QTL were linked to growth rate, yield, and yield component traits under both control and saline conditions, and leaf tissue ion accumulation under salt stress. Residuals from regressions fitting best linear unbiased predictions from saline conditions onto best linear unbiased predictions from control conditions provided a measure of salinity tolerance per se, independent of yield potential. Six QTL on CaLG04, CaLG05, and CaLG06 were associated with tolerance per se. In total, 21 QTL mapped to two distinct regions on CaLG04. The first distinct region controlled the number of filled pods, leaf necrosis, seed number, and seed yield specifically under salinity, and co-located with four QTL linked to salt tolerance per se. The second distinct region controlled 100-seed weight and growth-related traits, independent of salinity treatment. Positional cloning of the salinity tolerance-specific loci on CaLG04, CaLG05, and CaLG06 will improve our understanding of the key determinants of salinity tolerance in chickpea.