Origin and evolution of the nuclear auxin response system

Across all kingdoms of life, signaling molecules like hormones, for example, control many aspects of the lives of organisms, including how they grow and develop. Cells have dedicated proteins that can recognize the signaling molecules, relay the information, and respond to the signal, for example by switching genes on or off. Such response systems usually consist of multiple components, and, throughout evolution, these response components have regularly been copied such that many species have multiple different versions of each one. Auxin is a plant hormone that controls virtually all growth and developmental processes in plants, including many yield traits in crops. However, no one knows why it is involved in so many processes. This is partly because it is not clear how the response system for this central signaling molecule was first born, or how it has increased in its complexity. To address this, Mutte, Kato et al. explored the genetic information of more than a thousand plant species, including algae, which span more than 700 million years of evolution. Their analysis showed that all auxin response components were assembled from pieces of much older genes, but that they first came together when plants conquered land. Indeed, the auxin response appears to have developed on top of a pre-existing genetic regulator that is still present in modern-day algae. Mutte, Kato et al. then used experiments to show how stepwise increases in the number and types of auxin response components have shaped sophisticated, complex responses in land plants, and to demonstrate how ancient components control auxin response. Together these findings provide a framework for understanding the many functions of auxin in plants, and how this came to be. They also show how complexity can be accomplished in a signal response pathway, and how diversity evolves in gene families. Similar studies on other response systems in plants and beyond are likely to help reveal common principles of hormone response evolution and diversification of gene regulation systems.