Functional innovations of PIN auxin transporters mark crucial evolutionary transitions during rise of flowering plants.

Abstract

Flowering plants display the highest diversity among plant species and have notably shaped terrestrial landscapes. Nonetheless, the evolutionary origin of their unprecedented morphological complexity remains largely an enigma. Here, we show that the coevolution of cis-regulatory and coding regions of <i>PIN-FORMED</i> (<i>PIN</i>) auxin transporters confined their expression to certain cell types and directed their subcellular localization to particular cell sides, which together enabled dynamic auxin gradients across tissues critical to the complex architecture of flowering plants. Extensive intraspecies and interspecies genetic complementation experiments with <i>PIN</i>s from green alga up to flowering plant lineages showed that <i>PIN</i> genes underwent three subsequent, critical evolutionary innovations and thus acquired a triple function to regulate the development of three essential components of the flowering plant <i>Arabidopsis</i>: shoot/root, inflorescence, and floral organ. Our work highlights the critical role of functional innovations within the <i>PIN</i> gene family as essential prerequisites for the origin of flowering plants.