Negative regulation of conserved <i>RSL</i> class I bHLH transcription factors evolved independently among land plants.

Abstract

Basic helix-loop-helix transcription factors encoded by <i>RSL</i> 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 <i>Arabidopsis thaliana</i>. To find negative regulators of <i>RSL</i> class I genes in early diverging land plants we conducted a mutant screen in the liverwort <i>Marchantia polymorpha</i>. This identified FEW RHIZOIDS1 (MpFRH1) microRNA (miRNA) that negatively regulates the <i>RSL</i> class I gene Mp<i>RSL1</i>. The miRNA and its mRNA target constitute a feedback mechanism that controls epidermal cell differentiation. MpFRH1 miRNA target sites are conserved among liverwort <i>RSL</i> class I mRNAs but are not present in <i>RSL</i> class I mRNAs of other land plants. These findings indicate that while <i>RSL</i> class I genes are ancient and conserved, independent negative regulatory mechanisms evolved in different lineages during land plant evolution.