Water‐related innovations in land plants evolved by different patterns of gene cooption and novelty

Abstract

The origin of land plants and their descendants was marked by the evolution of key adaptations to life in terrestrial environments such as roots, vascular tissue and stomata. Though these innovations are well characterized, the evolution of the genetic toolkit underlying their development and function is poorly understood. We analysed molecular data from 532 species to investigate the evolutionary origin and diversification of genes involved in the development and regulation of these adaptations. We show that novel genes in the first land plants led to the single origin of stomata, but the stomatal closure of seed plants resulted from later gene expansions. By contrast, the major mechanism leading to the origin of vascular tissue was cooption of genes that emerged in the first land plants, enabling continuous water transport throughout the ancestral vascular plant. In turn, new key genes in the ancestors of plants with true leaves and seed plants led to the emergence of roots and lateral roots. The analysis highlights the different modes of evolution that enabled plants to conquer land, suggesting that gene expansion and cooption are the most common mechanisms of biological innovation in plant evolutionary history.