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A transcription factor module regulating stomatal formation is co-opted for the development of setae in the astomatous liverwort Marchantia polymorpha

View ORCID ProfileKenta C. Moriya, Makoto Shirakawa, Jeanne Loue-Manifel, Yoriko Matsuda, View ORCID ProfileKentaro Tamura, View ORCID ProfileYoshito Oka, View ORCID ProfileTomonao Matsushita, View ORCID ProfileIkuko Hara-Nishimura, View ORCID ProfileGwyneth Ingram, View ORCID ProfileRyuichi Nishihama, View ORCID ProfileJustin Goodrich, View ORCID ProfileTakayuki Kohchi, View ORCID ProfileTomoo Shimada
doi: https://doi.org/10.1101/2022.04.29.489008
Kenta C. Moriya
1Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan
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Makoto Shirakawa
2Graduate School of Biological Sciences, Nara Institute of Science and Technology (NAIST), Ikoma 630-0192, Japan
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Jeanne Loue-Manifel
3Laboratoire Reproduction et Développement des Plantes, University of Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Lyon 69342, France
4Institute of Molecular Plant Sciences, University of Edinburgh, Daniel Rutherford Building, Max Born Crescent, Edinburgh EH9 3BF, UK
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Yoriko Matsuda
5Graduate School of Biostudies, Kyoto University, Kyoto 606-8502, Japan
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Kentaro Tamura
6School of Food and Nutritional Sciences, University of Shizuoka, Shizuoka 422-8526, Japan
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Yoshito Oka
1Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan
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Tomonao Matsushita
1Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan
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Ikuko Hara-Nishimura
7Faculty of Science and Engineering, Konan University, Kobe 658-8501, Japan
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Gwyneth Ingram
3Laboratoire Reproduction et Développement des Plantes, University of Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Lyon 69342, France
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Ryuichi Nishihama
5Graduate School of Biostudies, Kyoto University, Kyoto 606-8502, Japan
8Department of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science, Noda 278-8510, Japan
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Justin Goodrich
4Institute of Molecular Plant Sciences, University of Edinburgh, Daniel Rutherford Building, Max Born Crescent, Edinburgh EH9 3BF, UK
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Takayuki Kohchi
5Graduate School of Biostudies, Kyoto University, Kyoto 606-8502, Japan
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Tomoo Shimada
1Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan
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  • For correspondence: tshimada@gr.bot.kyoto-u.ac.jp
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Abstract

The evolution of special types of cells requires the acquisition of new gene regulatory networks controlled by transcription factors (TFs). In stomatous plants, the stomatal formation is regulated by a TF module formed by subfamilies Ia and IIIb basic helix-loop-helix TFs (Ia-IIIb bHLH); however, how this module evolved during land plant diversification remains obscure. Here, we show that, in the astomatous liverwort Marchantia polymorpha, a Ia-IIIb bHLH module regulates the development of a unique sporophyte tissue, the setae, which are found in mosses and liverworts. The sole Ia bHLH gene, MpSETA, and a IIIb bHLH gene, MpICE2, regulate cell division and/or differentiation of seta lineage cells. MpSETA can partially replace the stomatal function of Ia bHLH TFs in Arabidopsis thaliana, suggesting the common regulatory mechanism underlying setal and stomatal formation. Our findings reveal the co-option of a Ia-IIIb bHLH TF module for regulating the cell fate determination and/or cell division of distinct types of cells during the evolution of land plant.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 01, 2022.
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A transcription factor module regulating stomatal formation is co-opted for the development of setae in the astomatous liverwort Marchantia polymorpha
Kenta C. Moriya, Makoto Shirakawa, Jeanne Loue-Manifel, Yoriko Matsuda, Kentaro Tamura, Yoshito Oka, Tomonao Matsushita, Ikuko Hara-Nishimura, Gwyneth Ingram, Ryuichi Nishihama, Justin Goodrich, Takayuki Kohchi, Tomoo Shimada
bioRxiv 2022.04.29.489008; doi: https://doi.org/10.1101/2022.04.29.489008
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A transcription factor module regulating stomatal formation is co-opted for the development of setae in the astomatous liverwort Marchantia polymorpha
Kenta C. Moriya, Makoto Shirakawa, Jeanne Loue-Manifel, Yoriko Matsuda, Kentaro Tamura, Yoshito Oka, Tomonao Matsushita, Ikuko Hara-Nishimura, Gwyneth Ingram, Ryuichi Nishihama, Justin Goodrich, Takayuki Kohchi, Tomoo Shimada
bioRxiv 2022.04.29.489008; doi: https://doi.org/10.1101/2022.04.29.489008

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