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

Research output: Contribution to journalArticleResearchpeer-review

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

Cite this

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. / Class C ARFs evolved before the origin of land plants and antagonize differentiation and developmental transitions in Marchantia polymorpha. In: New Phytologist. 2018 ; Vol. 218, No. 4. pp. 1612-1630.
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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.",
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Class C ARFs evolved before the origin of land plants and antagonize differentiation and developmental transitions in Marchantia polymorpha. / 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.

In: New Phytologist, Vol. 218, No. 4, 01.06.2018, p. 1612-1630.

Research output: Contribution to journalArticleResearchpeer-review

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T1 - Class C ARFs evolved before the origin of land plants and antagonize differentiation and developmental transitions in Marchantia polymorpha

AU - Flores-Sandoval, Eduardo

AU - Eklund, D. Magnus

AU - Hong, Syuan Fei

AU - Alvarez, John P.

AU - Fisher, Tom J.

AU - Lampugnani, Edwin R.

AU - Golz, John F.

AU - Vázquez-Lobo, Alejandra

AU - Dierschke, Tom

AU - Lin, Shih Shun

AU - Bowman, John L

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