The phylotranscriptomic profile of angiosperm seed development follows a reverse hourglass pattern

The angiosperm seed life cycle encompasses three broad phases-embryogenesis, maturation, and germination. Seed maturation is particularly critical, bridging embryo development and germination while enabling accumulation of nutrient reserves and acquisition of traits like desiccation tolerance, essential for survival in diverse environments. While embryogenesis and germination in Arabidopsis thaliana are known to follow an hourglass-like phylotranscriptomic pattern (with higher gene expression conservation in the mid-stages), the transcriptomic landscape of seed maturation and the complete seed life cycle remain unexplored. Using publicly available RNA-seq data, we generated transcriptome age index and transcriptome divergence index profiles of all three phases of the Arabidopsis seed life cycle, revealing a reverse hourglass-like phylotranscriptome pattern. Seed maturation exhibited increased expression of younger genes with divergent expression patterns compared to embryogenesis and germination, which was conserved in other dicots and monocots. Tissue-specific analyses revealed that, in monocots, the endosperm has increased expression of younger genes during maturation. We found that, similar to pollen development, seed maturation is a pivotal phase enabling the expression of young, rapidly evolving genes. We propose the "out of the seed" hypothesis, where seed maturation serves as a landscape for expressing new genes and promoting functional specialization.