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New Phytol. 2018 Jun;218(4):1612-1630. doi: 10.1111/nph.15090. Epub 2018 Mar 25.

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

Author information

1
School of Biological Sciences, Monash University, Clayton, Melbourne, Victoria, 3800, Australia.
2
Institute of Biotechnology, National Taiwan University, 81, Chang-Xing ST., Taipei, 106, Taiwan.
3
School of BioSciences, University of Melbourne, Parkville, Victoria, 3010, Australia.
4
CIByC, Universidad Autónoma del Estado de Morelos, Av. Universidad No. 1001, Colonia Chamilpa, CP 62209, Cuernavaca, Morelos, México.

Abstract

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.

KEYWORDS:

Marchantia ; AUXIN RESPONSE FACTOR (ARF); auxin; auxin signalling; class C ARF; land plant evolution; mir160

PMID:
29574879
DOI:
10.1111/nph.15090

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