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

• Published in: The New phytologist Vol. 218; no. 4; pp. 1612 - 1630
• Main Authors: Flores‐Sandoval, Eduardo, Eklund, D. Magnus, Hong, Syuan‐Fei, Alvarez, John P., Fisher, Tom J., Lampugnani, Edwin R., Golz, John F., Vázquez‐Lobo, Alejandra, Dierschke, Tom, Lin, Shih‐Shun, Bowman, John L.
• Format: Journal Article
• Language: English
• Published: England New Phytologist Trust 01.06.2018; Wiley Subscription Services, Inc
• Subjects: Acetic acid; Algae; Alleles; auxin; AUXIN RESPONSE FACTOR (ARF); auxin signalling; Auxins; class C ARF; Differentiation; Gametophytes; Gene expression; Genes; Indoleacetic acid; Innovation; Innovations; land plant evolution; Life cycle; Life cycle engineering; Life cycles; Marchantia; Marchantia polymorpha; mir160; Phylogenetics; Phylogeny; Transcription; AUXIN RESPONSE FACTOR (ARF); auxin; land plant evolution; auxin signalling; class C ARF; mir160; Marchantia
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.15090

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 auxinin-sensitive, 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.