Diverse branching forms regulated by a core auxin transport mechanism in plants

Abstract

Diverse branching forms have evolved multiple times across the tree of life to facilitate resource acquisition and exchange with the environment. In land plants, sporophyte branching enabled the diversification of the dominant vascular plant clade and arose in their last shared common ancestor; the bryophyte sisters to vascular plants are unbranched. Mechanisms for sporophyte branching are well known in Arabidopsis, where branch initiation and plastic branch outgrowth require directional auxin transport by PIN proteins. However, no broadly applicable genetic mechanisms for branching in vascular plants are known. We have used a combination of surgical and pharmacological treatments and PIN expression analyses in the lycophyte Selaginella kraussiana to identify PIN-mediated auxin transport as the ancestral mechanism for branching within vascular plants. We show that short-range auxin transport out of the shoot tips promotes branching, and that branch dominance is coordinated by long-range auxin transport throughout the shoot system. Moreover, the plastic outgrowth of a branch from a unique organ system innovated in lycophytes (the rhizophore) is regulated by long-range auxin transport and associated with a transitory drop in PIN expression. We conclude that an ancestral mechanism for branching was independently recruited into plastic branch outgrowth in lycophytes and seed plants. Considered in conjunction with data from other species, our results highlight a pivotal role for the co-option of PINs into the evolution of branching in diverse plant forms.