Abstract

Summary Armadillo‐related proteins regulate development throughout eukaryotic kingdoms. In the flowering plant Arabidopsis thaliana, Armadillo‐related ARABIDILLO proteins promote multicellular root branching. ARABIDILLO homologues exist throughout land plants, including early‐diverging species lacking true roots, suggesting that early‐evolving ARABIDILLOs had additional biological roles.Here we investigated, using molecular genetics, the conservation and diversification of ARABIDILLO protein function in plants separated by c. 450 million years of evolution.We demonstrate that ARABIDILLO homologues in the moss Physcomitrella patens regulate a previously undiscovered inhibitory effect of abscisic acid (ABA) on spore germination. Furthermore, we show that A. thaliana ARABIDILLOs function similarly during seed germination. Early‐diverging ARABIDILLO homologues from both P. patens and the lycophyte Selaginella moellendorffii can substitute for ARABIDILLO function during A. thaliana root development and seed germination.We conclude that (1) ABA was co‐opted early in plant evolution to regulate functionally analogous processes in spore‐ and seed‐producing plants and (2) plant ARABIDILLO germination functions were co‐opted early into both gametophyte and sporophyte, with a specific rooting function evolving later in the land plant lineage.

Highlights

  • Plant lifecycles undergo an alternation of generations between a haploid gametophyte and a diploid sporophyte phase (Hofmeister, 1851)

  • We investigated, using molecular genetics, the conservation and diversification of ARABIDILLO protein function in plants separated by c. 450 million years of evolution

  • We demonstrate that ARABIDILLO homologues in the moss Physcomitrella patens regulate a previously undiscovered inhibitory effect of abscisic acid (ABA) on spore germination

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Summary

Introduction

Plant lifecycles undergo an alternation of generations between a haploid gametophyte and a diploid sporophyte phase (Hofmeister, 1851). The moss Physcomitrella patens (Prigge & Bezanilla, 2010) and liverwort Marchantia polymorpha (Shimamura, 2015), has demonstrated that rhizoid development has mechanistic similarity with the development of epidermal root hairs on the multicellular roots of the flowering plant Arabidopsis thaliana (Menand et al, 2007; Proust et al, 2016) This suggests that nonhomologous, but functionally similar, epidermal structures (i.e. tip-growing cells with a rooting function) are regulated by genes that were co-opted into both gametophyte and sporophyte (Menand et al, 2007; Proust et al, 2016). It is likely that a ‘rewiring’ of the root hair/rhizoid gene regulatory network occurred between the bryophyte gametophyte and the flowering plant sporophyte (Yi et al, 2010; Jang & Dolan, 2011; Jang et al, 2011; Pires et al, 2013; Tam et al, 2015)

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