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A Simple Auxin Transcriptional Response System Regulates Multiple Morphogenetic Processes in the Liverwort Marchantia polymorpha

Journal Article · · PLoS Genetics
 [1];  [2];  [3];
  1. Monash Univ., Melbourne, VIC (Australia). School of Biological Sciences; DOE/OSTI
  2. Monash Univ., Melbourne, VIC (Australia). School of Biological Sciences
  3. Monash Univ., Melbourne, VIC (Australia). School of Biological Sciences; Uppsala Univ. (Sweden). Evolutionary Biology Centre. Dept. of Plant Ecology and Evolution
In land plants comparative genomics has revealed that members of basal lineages share a common set of transcription factors with the derived flowering plants, despite sharing few homologous structures. The plant hormone auxin has been implicated in many facets of development in both basal and derived lineages of land plants. We functionally characterized the auxin transcriptional response machinery in the liverwort Marchantia polymorpha, a member of the basal lineage of extant land plants. All components known from flowering plant systems are present in M. polymorpha, but they exist as single orthologs: a single MpTOPLESS (TPL) corepressor, a single MpTRANSPORT INHIBITOR RESPONSE 1 auxin receptor, single orthologs of each class of AUXIN RESPONSE FACTOR (ARF; MpARF1, MpARF2, MpARF3), and a single negative regulator AUXIN/INDOLE-3-ACETIC ACID (MpIAA). Phylogenetic analyses suggest this simple system is the ancestral condition for land plants. We experimentally demonstrate that these genes act in an auxin response pathway — chimeric fusions of the MpTPL corepressor with heterodimerization domains of MpARF1, MpARF2, or their negative regulator, MpIAA, generate auxin insensitive plants that lack the capacity to pattern and transition into mature stages of development. Our results indicate auxin mediated transcriptional regulation acts as a facilitator of branching, differentiation and growth, rather than acting to determine or specify tissues during the haploid stage of the M. polymorpha life cycle. We hypothesize that the ancestral role of auxin is to modulate a balance of differentiated and pluri- or totipotent cell states, whose fates are determined by interactions with combinations of unrelated transcription factors.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1627308
Journal Information:
PLoS Genetics, Journal Name: PLoS Genetics Journal Issue: 5 Vol. 11; ISSN 1553-7404
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

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Origin and evolution of the nuclear auxin response system posted_content November 2017
Efficient CRISPR/Cas9-based genome editing and its application to conditional genetic analysis in Marchantia polymorpha posted_content March 2018
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Regional Growth Rate Differences Specified by Apical Notch Activities Regulate Liverwort Thallus Shape journalarticle January 2017
Improved Monitoring of Low-Level Transcription in Escherichia coli by a β-Galactosidase α-Complementation System journal June 2019
Ferns: the missing link in shoot evolution and development journal November 2015
Co-expression and Transcriptome Analysis of Marchantia polymorpha Transcription Factors Supports Class C ARFs as Independent Actors of an Ancient Auxin Regulatory Module journal October 2018
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The Evolution of Flavonoid Biosynthesis: A Bryophyte Perspective journal February 2020
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Constitutive auxin response in Physcomitrella reveals complex interactions between Aux/IAA and ARF proteins journal June 2016
Flexibility of intrinsically disordered degrons in AUX/IAA proteins reinforces auxin co-receptor assemblies journal May 2020
Evolution of land plants: insights from molecular studies on basal lineages journal January 2017
Evolution of nuclear auxin signaling: lessons from genetic studies with basal land plants journal August 2017
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The Roles of the Sole Activator-Type Auxin Response Factor in Pattern Formation of Marchantia polymorpha journal July 2017
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Loss of CG methylation in Marchantia Polymorpha causes disorganization of cell division and reveals unique DNA methylation regulatory mechanisms of non-CG methylation posted_content July 2018
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Flexibility of intrinsically disordered degrons in AUX/IAA proteins reinforces auxin co-receptor assemblies posted_content October 2019
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