Developmental phylotranscriptomics in grapevine suggests an ancestral role of somatic embryogenesis.

Abstract

The zygotic embryogenesis of Arabidopsis, which is initiated by gamete fusion, shows hourglass-shaped ontogeny-phylogeny correlations at the transcriptome level. However, many plants are capable of yielding a fully viable next generation by somatic embryogenesis-a comparable developmental process that usually starts with the embryogenic induction of a diploid somatic cell. To explore the correspondence between ontogeny and phylogeny in this alternative developmental route in plants, here we develop a highly efficient model of somatic embryogenesis in grapevine (Vitis vinifera) and sequence its developmental transcriptomes. By combining the evolutionary properties of grapevine genes with their expression values, recovered from early induction to the formation of juvenile plants, we find a strongly supported hourglass-shaped developmental trajectory. However, in contrast to zygotic embryogenesis in Arabidopsis, where the torpedo stage is the most evolutionarily inert, in the somatic embryogenesis of grapevine, the heart stage expresses the most evolutionarily conserved transcriptome. This represents a surprising finding because it suggests a better evolutionary system-level analogy between animal development and plant somatic embryogenesis than zygotic embryogenesis. We conclude that macroevolutionary logic is deeply hardwired in plant ontogeny and that somatic embryogenesis is likely a primordial embryogenic program in plants.