Co-option of plant gene regulatory network in nutrient responses during terrestrialization

Abstract

Plant responses to nitrate, phosphate and sucrose form a complex molecular network crucial for terrestrial adaptation. However, the origins, functional diversity and evolvability of this network during plant terrestrialization remain scarcely understood. Here we compare the transcriptomic response to these nutrients in the bryophyte Marchantia polymorpha and the streptophyte alga Klebsormidium nitens. We show that the largely species-specific nutrient response pattern is driven by gene regulatory network (GRN) alterations. Intriguingly, while pathways governing the GRNs exhibit modest conservation, M. polymorpha GRNs exhibit more regulatory connections through the redeployment of ancient transcription factor CSD. In M. polymorpha, functional analyses reveal the involvement of pre-existing cytokinin machineries in downstream targets, orchestrating plastic morpho-physiological responses to nutrient status. Our findings implicate the genetic co-option events facilitating successful land plant establishment.