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

Flores-Sandoval, Eduardo; Eklund, D. Magnus; Bowman, John L.; Bomblies, Kirsten

doi:10.1371/journal.pgen.1005207

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

Journal Article · Thu May 28 00:00:00 EDT 2015 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1005207· OSTI ID:1627308

Flores-Sandoval, Eduardo ^[1]; Eklund, D. Magnus ^[1]; Bowman, John L. ^[2]; Bomblies, Kirsten

Monash Univ., Melbourne, VIC (Australia). School of Biological Sciences
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.

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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, Vol. 11, Issue 5; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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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 Ikeda, Yoko; Nishihama, Ryuichi; Yamaoka, Shohei Plant and Cell Physiology https://doi.org/10.1093/pcp/pcy161	journal	August 2018
Evolution of strigolactone receptors by gradual neo-functionalization of KAI2 paralogues Bythell-Douglas, Rohan; Rothfels, Carl J.; Stevenson, Dennis W. D. BMC Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12915-017-0397-z	journal	June 2017
Loop assembly: a simple and open system for recursive fabrication of DNA circuits. Pollak, Bernardo; Cerda, Ariel; Delmans, Mihails Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.34858	text	January 2019
Extensive epigenetic reprogramming during the life cycle of Marchantia polymorpha W., Schmid, Marc; Alejandro, Giraldo-Fonseca,; Moritz, Rövekamp, BioMed Central https://doi.org/10.5167/uzh-165512	text	January 2018
Origin and evolution of the nuclear auxin response system Mutte, Sumanth K.; Kato, Hirotaka; Rothfels, Carl bioRxiv https://doi.org/10.1101/220731	posted_content	November 2017
Flexibility of intrinsically disordered degrons in AUX/IAA proteins reinforces auxin co-receptor assemblies Niemeyer, Michael; Moreno Castillo, Elena; Ihling, Christian H. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16147-2	journal	May 2020
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The Rise of Evolutionary Molecular Plant–Microbe Interactions (EvoMPMI) Betsuyaku, Shigeyuki Plant and Cell Physiology, Vol. 61, Issue 2 https://doi.org/10.1093/pcp/pcaa007	journal	February 2020
Correction: A Simple Auxin Transcriptional Response System Regulates Multiple Morphogenetic Processes in the Liverwort Marchantia polymorpha Flores-Sandoval, Eduardo; Eklund, D. Magnus; Bowman, John L. PLOS Genetics, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pgen.1005900	journal	February 2016
Regional Growth Rate Differences Specified by Apical Notch Activities Regulate Liverwort Thallus Shape Solly, Je; Cunniffe, Nj; Harrison, Cj Elsevier https://doi.org/10.17863/cam.7245	journalarticle	January 2017
Ferns: the missing link in shoot evolution and development Plackett, Andrew R. G.; Di Stilio, Verónica S.; Langdale, Jane A. Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00972	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 Flores-Sandoval, Eduardo; Romani, Facundo; Bowman, John L. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01345	journal	October 2018
Non-destructive Plant Morphometric and Color Analyses Using an Optoelectronic 3D Color Microscope Lazcano-Ramírez, Hugo G.; Gómez-Felipe, Andrea; Díaz-Ramírez, David Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01409	journal	September 2018
The Evolution of Flavonoid Biosynthesis: A Bryophyte Perspective Davies, Kevin M.; Jibran, Rubina; Zhou, Yanfei Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.00007	journal	February 2020

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