Transcriptome and translatome profiling and translational network analysis during seed maturation reveals conserved transcriptional and distinct translational regulatory patterns

Abstract

Seed maturation is an important plant developmental process that follows embryo development. It is associated with a series of physiological changes such as the establishment of desiccation tolerance, seed longevity and seed dormancy. However, the translational dynamics associated with seed maturation, especially its connection with seed germination remains largely elusive. Here transcriptome and translatome profiling were performed during seed maturation. During seed maturation we observed a gradual disappearance of polysomes and a relative increase of monosomes, indicating a gradual reduction of global translation. Comparing the levels of polysomal associated mRNAs with total mRNA levels showed that thousands of genes are translationally regulated at early sates of maturation, as judged by dramatic changes in polysomal occupancy. By including previous published data from germination and seedling establishment, a translational regulatory network: SeedTransNet was constructed. Network analysis identified hundreds of gene modules with distinct functions and transcript sequence features indicating the existence of separate translational regulatory circuits possibly acting through specific regulatory elements. The regulatory potential of one such element was confirmed in vivo. The network identified several seed maturation associated genes as central nodes, and we could confirm the importance of many of these hub genes with a maturation associated seed phenotype by mutant analysis. One of the identified regulators an AWPM19 family protein PM19-Like1 (PM19L1) was shown to regulate seed dormancy and longevity. This putative RBP also affects the transitional regulation of one its, by the SeedTransNet identified, target mRNAs. Our data shows the usefulness of SeedTransNet in identifying regulatory pathways during seed phase transitions.