Genetic determinants of seed protein plasticity in response to the environment in Medicago truncatula

SUMMARY As the frequency of extreme environmental events is expected to increase with climate change, identifying candidate genes for stabilizing the protein composition of legume seeds or optimizing this in a given environment is increasingly important. To elucidate the genetic determinants of seed protein plasticity, major seed proteins from 200 ecotypes of Medicago truncatula grown in four contrasting environments were quantified after one‐dimensional electrophoresis. The plasticity index of these proteins was recorded for each genotype as the slope of Finlay and Wilkinson's regression and then used for genome‐wide association studies (GWASs), enabling the identification of candidate genes for determining this plasticity. This list was enriched in genes related to transcription, DNA repair and signal transduction, with many of them being stress responsive. Other over‐represented genes were related to sulfur and aspartate family pathways leading to the synthesis of the nutritionally essential amino acids methionine and lysine. By placing these genes in metabolic pathways, and using a M. truncatula mutant impaired in regenerating methionine from S‐methylmethionine, we discovered that methionine recycling pathways are major contributors to globulin composition establishment and plasticity. These data provide a unique resource of genes that can be targeted to mitigate negative impacts of environmental stresses on seed protein composition. Significance Statement In the context of climate change, legumes that produce seeds with high protein contents without nitrogen fertilizer are vital for human and livestock nutrition. Thus, optimizing and stabilizing their seed protein yield and composition is of crucial importance. GWASs using the natural genetic variation of Medicago truncatula showed that methionine recycling pathways are major determinants of the plastic response of seed protein composition to environmental changes.