Genome-Wide Association Studies of Seed Performance Traits in Response to Heat Stress in Medicago truncatula Uncover MIEL1 as a Regulator of Seed Germination Plasticity

Legume seeds are an important source of proteins, minerals, and vitamins for human and animal diets and represent a keystone for food security. With climate change and global warming, the production of grain legumes faces new challenges concerning seed vigor traits that allow the fast and homogenous establishment of the crop in a wide range of environments. These seed performance traits are regulated during seed maturation and are under the strong influence of the maternal environment. In this study, we used 200 natural Medicago truncatula accessions, a model species of legumes grown in optimal conditions and under moderate heat stress (26 degrees C) during seed development and maturation. This moderate stress applied at flowering onwards impacted seed weight and germination capacity. Genome-wide association studies (GWAS) were performed to identify putative loci or genes involved in regulating seed traits and their plasticity in response to heat stress. We identified numerous significant quantitative trait nucleotides and potential candidate genes involved in regulating these traits under heat stress by using post-GWAS analyses combined with transcriptomic data. Out of them, MtMIEL1, a RING-type zinc finger family gene, was shown to be highly associated with germination speed in heat-stressed seeds. In Medicago, we highlighted that MtMIEL1 was transcriptionally regulated in heat-stressed seed production and that its expression profile was associated with germination speed in different Medicago accessions. Finally, a loss-of-function analysis of the Arabidopsis MIEL1 ortholog revealed its role as a regulator of germination plasticity of seeds in response to heat stress.

Automated summary

Legume seeds are crucial sources of proteins, minerals, and vitamins for human and animal diets, and their performance traits are influenced by the maternal environment. Heat stress during seed development can impact seed weight and germination capacity, with genome-wide association studies identifying potential genes involved in regulating these traits. MtMIEL1, a zinc finger family gene, was found to be associated with germination speed in heat-stressed seeds, highlighting its role in regulating seed traits under stress conditions.