Abstract
Seed mass is a key component of adaptation in plants and a determinant of yield in crops. The climatic drivers and genomic basis of seed mass variation remain poorly understood. In the cereal crop Sorghum bicolor, globally-distributed landraces harbor abundant variation in seed mass, which is associated with precipitation in their agroclimatic zones of origin. This study aimed to test the hypothesis that diversifying selection across precipitation gradients, acting on ancestral cereal grain size regulators, underlies seed mass variation in global sorghum germplasm. We tested this hypothesis in a set of 1901 georeferenced and genotyped sorghum landraces, 100-seed mass from common gardens, and bioclimatic precipitation variables. As predicted, 100-seed mass in global germplasm varies significantly among botanical races and is correlated to proxies of the precipitation gradients. With general and mixed linear model genome-wide associations, we identified 29 and 56 of 100 a priori candidate seed size genes with polymorphisms in the top 1% of seed mass association, respectively. Eleven of these genes harbor polymorphisms associated with the precipitation gradient, including orthologs of genes that regulate seed size in other cereals. With FarmCPU, 13 significant SNPs were identified, including one at an a priori candidate gene. Finally, we identified eleven colocalized outlier SNPs associated with seed mass and precipitation that also carry signatures of selection based on FST scans and PCAdapt, which represents a significant enrichment. Our findings suggest that seed mass in sorghum was shaped by diversifying selection on drought stress, and can inform genomics-enabled breeding for climate-resilient cereals.
Highlights
Local adaptation exists when the average fitness of organisms in their local environment is higher than conspecifics from other environments (Des Marais et al 2013; Blanquart et al 2013)
Seed size was estimated for 1901 sorghum landraces using 100-seed mass obtained from the US National Plant Germplasm System’s Germplasm Resources Information Network (GRIN) or the International Crops Research Institute for the Semi-Arid Tropics (ICRISAT) genebanks (Table S1)
To account for the effect of location, best linear unbiased predictors (BLUPs) of 100seed mass from the two genebanks were estimated for all accessions using a random linear model implemented in R package lme4 (Bates et al 2015) as follows: yij 1⁄4 μ þ Gi þ Ej þ εij where yij is the 100-seed mass of the ith accession in the jth location, μ is the overall mean, Gi is the random genotypic effect for the ith accession, Ej is the random environmental effect of the jth location, and εij is the residual
Summary
Local adaptation exists when the average fitness of organisms in their local environment is higher than conspecifics from other environments (Des Marais et al 2013; Blanquart et al 2013). Life-history theory suggests a trade-off between seed mass and seed number, given a constant amount of available resources to produce the seeds (Smith and Fretwell 1974). Increasing seed size provides more reserves for seedling growth, but greater number of seeds provides more propagules and bet-hedging (Olofsson et al 2009). In semi-arid and arid regions, precipitation-mediated water availability may act as a selective pressure on seed size (Hallett et al 2011), but findings on seed size adaptation to drought risk have been contradictory (Leishman et al 2000). In crops, which evolve under both natural and artificial selection, grain size is a main component determining grain yield, subject to similar ecophysiological trade-offs (Sadras 2007)
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