Inference of longevity-related genes from a robust co-expression network of seed maturation identifies new regulators linking seed storability to biotic defense-related pathways

Seed longevity, the maintenance of viability during storage is a crucial factor to preserve genetic resources and to ensure proper seedling establishment and high crop yield. A systems biology approach was used to identify key genes regulating the acquisition of longevity during seed maturation of Medicago truncatula. Using 104 transcriptomes of seed developmental time courses obtained under five growth environments, a robust, stable co-expression network (MatNet) was generated, thereby capturing the conserved backbone of maturation. Using a trait-based gene significance measure, a co-expression module related to the acquisition of longevity was inferred from MatNet. Comparative analysis between maturation processes in Medicago and A. thaliana seeds and mining Arabidopsis interaction databases revealed conserved connectivity for 87% of longevity module nodes between both species. Arabidopsis mutant screening for longevity and maturation phenotypes demonstrated high predictive power of the longevity cross-species network. Overrepresentation analysis of the network nodes indicated biological functions related to defense, light and auxin. Characterization of defense-related wrky3 and nfxl1 mutants demonstrated that these genes regulate part of the network nodes and exhibit impaired longevity acquisition during maturation. These data suggest that seed longevity evolved by co-opting existing genetic pathways regulating activation of defense against pathogens.