Abstract

An important adaptation during colonization of land by plants is gravitropic growth of roots, which enabled roots to reach water and nutrients, and firmly anchor plants in the ground. Here we provide insights into the evolution of an efficient root gravitropic mechanism in the seed plants. Architectural innovation, with gravity perception constrained in the root tips along with a shootward transport route for the phytohormone auxin, appeared only upon the emergence of seed plants. Interspecies complementation and protein domain swapping revealed functional innovations within the PIN family of auxin transporters leading to the evolution of gravitropism-specific PINs. The unique apical/shootward subcellular localization of PIN proteins is the major evolutionary innovation that connected the anatomically separated sites of gravity perception and growth response via the mobile auxin signal. We conclude that the crucial anatomical and functional components emerged hand-in-hand to facilitate the evolution of fast gravitropic response, which is one of the major adaptations of seed plants to dry land.

Highlights

  • An important adaptation during colonization of land by plants is gravitropic growth of roots, which enabled roots to reach water and nutrients, and firmly anchor plants in the ground

  • To obtain a broad view of the evolutionary origin of root gravitropism, we selected various plant species representing the lineages of mosses, lycophytes, ferns, gymnosperms, and flowering plants, including dicots and monocots, and analyzed their root gravitropic response (Fig. 1)

  • In the basal seed plant gymnosperm P. taeda (Pt), we identified five PIN genes, distributed in the five clades of the PIN phylogeny[42], but domain prediction clearly indicated that the PtPINF protein is not complete

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Summary

Introduction

An important adaptation during colonization of land by plants is gravitropic growth of roots, which enabled roots to reach water and nutrients, and firmly anchor plants in the ground. Interspecies complementation and protein domain swapping revealed functional innovations within the PIN family of auxin transporters leading to the evolution of gravitropism-specific PINs. The unique apical/shootward subcellular localization of PIN proteins is the major evolutionary innovation that connected the anatomically separated sites of gravity perception and growth response via the mobile auxin signal. The fossil evidence indicates that the true roots emerged in the vascular plants[9], and in the flowering plants the root has evolved into an organ to grow downwards along the gravity vector with two main purposes: anchoring in the soil and providing a source of water and nutrients for growth of the above-ground parts of the plants[10]. Answering this fundamental question would reveal how, during plant evolutionary history, root evolved to be such an efficient device to respond to the Earth gravity

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