The advantages of crosstalk during the evolution of the BZR1-ARF6-PIF4 (BAP) module.

Abstract

The BAP module, comprising BRASSINAZOLE RESISTANT 1 (BZR1), AUXIN RESPONSE FACTOR 6 (ARF6), and PHYTOCHROME-INTERACTING FACTOR 4 (PIF4), functions as a molecular hub to orchestrate plant growth and development. In Arabidopsis thaliana, components of the BAP module physically interact to form a complex system that integrates light, brassinosteroid (BR), and auxin signals. Little is known about the origin and evolution of the BAP module. Here, we conducted comparative genomic and transcriptomic analyses to investigate the evolution and functional diversification of the BAP module. Our results suggest that the BAP module originated in land plants and that the ζ, ε, and γ whole-genome duplication/triplication events contributed to the expansion of BAP module components in seed plants. Comparative transcriptomic analysis suggested that the prototype BAP module arose in Marchantia polymorpha, experienced stepwise evolution, and became established as a mature regulatory system in seed plants. We developed a formula to calculate the signal transduction productivity of the BAP module and demonstrate that more crosstalk among components enables higher signal transduction efficiency. Our results reveal the evolutionary history of the BAP module and provide insights into the evolution of plant signaling networks and the strategies employed by plants to integrate environmental and endogenous signals.