Class C ARFs evolved before the origin of land plants and antagonize differentiation and developmental transitions in Marchantia polymorpha

• DOI: 10.1111/nph.15090
• Publication Date: 2018-03-25T17:36:15Z
• Authors: Eduardo Flores‐Sa...; D. Magnus Eklund; Syuan‐Fei Hong; John P. Alvarez; Tom J. Fisher; Edwin R. Lampugnani; John F. Golz; Alejandra Vázquez...; Tom Dierschke; Shih‐Shun Lin; John L. Bowman
• Keywords: Feedback, Physiological; Spores; 570; 0303 health sciences; Indoleacetic Acids; Transcription, Genetic; Plant Development; Cell Differentiation; 15. Life on land; Genes, Plant; Up-Regulation; Evolution, Molecular; MicroRNAs; 03 medical and health sciences; Phenotype; Protein Domains; Gene Expression Regulation, Plant; Multigene Family; Mutation; Marchantia; Alleles; Phylogeny; Plant Proteins; Signal Transduction

Summary

A plethora of developmental and physiological processes in land plants is influenced by auxin, to a large extent via alterations in gene expression by AUXIN RESPONSE FACTORs (ARFs). The canonical auxin transcriptional response system is a land plant innovation, however, charophycean algae possess orthologues of at least some classes of ARF and AUXIN/INDOLE‐3‐ACETIC ACID (AUX/IAA) genes, suggesting that elements of the canonical land plant system existed in an ancestral alga. We reconstructed the phylogenetic relationships between streptophyte ARF and AUX/IAA genes and functionally characterized the solitary class C ARF, MpARF3, in Marchantia polymorpha. Phylogenetic analyses indicate that multiple ARF classes, including class C ARFs, existed in an ancestral alga. Loss‐ and gain‐of‐function MpARF3 alleles result in pleiotropic effects in the gametophyte, with MpARF3 inhibiting differentiation and developmental transitions in multiple stages of the life cycle. Although loss‐of‐function Mparf3 and Mpmir160 alleles respond to exogenous auxin treatments, strong miR‐resistant MpARF3 alleles are auxin‐insensitive, suggesting that class C ARFs act in a context‐dependent fashion. We conclude that two modules independently evolved to regulate a pre‐existing ARF transcriptional network. Whereas the auxin‐TIR1‐AUX/IAA pathway evolved to repress class A/B ARF activity, miR160 evolved to repress class C ARFs in a dynamic fashion.