Abstract

Basic helix-loop-helix transcription factors encoded by RSL class I genes control a gene regulatory network that positively regulates the development of filamentous rooting cells - root hairs and rhizoids - in land plants. The GLABRA2 transcription factor negatively regulates these genes in the angiosperm Arabidopsis thaliana. To find negative regulators of RSL class I genes in early diverging land plants we conducted a mutant screen in the liverwort Marchantia polymorpha. This identified FEW RHIZOIDS1 (MpFRH1) microRNA (miRNA) that negatively regulates the RSL class I gene MpRSL1. The miRNA and its mRNA target constitute a feedback mechanism that controls epidermal cell differentiation. MpFRH1 miRNA target sites are conserved among liverwort RSL class I mRNAs but are not present in RSL class I mRNAs of other land plants. These findings indicate that while RSL class I genes are ancient and conserved, independent negative regulatory mechanisms evolved in different lineages during land plant evolution.

Highlights

  • Gene regulatory networks control differentiation of cells and tissues during development

  • The genetic program for the development of root hair cells and rhizoid cells is activated by functionally conserved basic helix-loop-helix transcription factors encoded by RSL class I genes

  • Land plant RSL class I genes control an ancient gene regulatory network that positively regulates the development of structures derived from single epidermal cells (Menand et al, 2007; Proust et al, 2016)

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Summary

Introduction

Gene regulatory networks control differentiation of cells and tissues during development. Changes in gene regulatory network structure are correlated with changes in morphology during the course of evolution. RSL class I genes promote root hair differentiation in the vascular plants rice (Oryza sativa), Brachypodium distachyon and Arabidopsis thaliana (Zalewski et al, 2013; Kim et al, 2017; Menand et al, 2007). Root hairs and rhizoids initiate from those epidermal cells that express RSL class I genes

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