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

Eduardo Flores-Sandoval, D. Magnus Eklund, Syuan Fei Hong, John P. Alvarez, Tom J. Fisher, Edwin R. Lampugnani, John F. Golz, Alejandra Vázquez-Lobo, Tom Dierschke, Shih Shun Lin, John L Bowman

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23 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)1612-1630
Number of pages19
JournalNew Phytologist
Volume218
Issue number4
DOIs
Publication statusPublished - 1 Jun 2018

Keywords

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

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Micromon

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Office of the Vice-Provost (Research and Research Infrastructure)

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Monash Micro Imaging

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Cite this

Flores-Sandoval, E., Eklund, D. M., Hong, S. F., Alvarez, J. P., Fisher, T. J., Lampugnani, E. R., Golz, J. F., Vázquez-Lobo, A., Dierschke, T., Lin, S. S., & Bowman, JL. (2018). Class C ARFs evolved before the origin of land plants and antagonize differentiation and developmental transitions in Marchantia polymorpha. New Phytologist, 218(4), 1612-1630. https://doi.org/10.1111/nph.15090