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An Ancestral Function of Strigolactones as Symbiotic Rhizosphere Signals

Kyoichi Kodama, Mélanie K. Rich, Akiyoshi Yoda, Shota Shimazaki, Xiaonan Xie, Kohki Akiyama, Yohei Mizuno, Aino Komatsu, Yi Luo, Hidemasa Suzuki, Hiromu Kameoka, Cyril Libourel, Jean Keller, Keiko Sakakibara, Tomoaki Nishiyama, Tomomi Nakagawa, Kiyoshi Mashiguchi, Kenichi Uchida, Kaori Yoneyama, Yoshikazu Tanaka, Shinjiro Yamaguchi, Masaki Shimamura, View ORCID ProfilePierre-Marc Delaux, View ORCID ProfileTakahito Nomura, View ORCID ProfileJunko Kyozuka
doi: https://doi.org/10.1101/2021.08.20.457034
Kyoichi Kodama
1Graduate School of Life Sciences, Tohoku University, Sendai, Japan
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Mélanie K. Rich
2LRSV, Université de Toulouse, CNRS, UPS, Toulouse INP, Auzeville-Tolosane, France
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Akiyoshi Yoda
3United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Tokyo, Japan
4Center for Bioscience Research and Education, Utsunomiya University, Tochigi, Japan
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Shota Shimazaki
1Graduate School of Life Sciences, Tohoku University, Sendai, Japan
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Xiaonan Xie
3United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Tokyo, Japan
4Center for Bioscience Research and Education, Utsunomiya University, Tochigi, Japan
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Kohki Akiyama
5Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Osaka, Japan
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Yohei Mizuno
1Graduate School of Life Sciences, Tohoku University, Sendai, Japan
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Aino Komatsu
1Graduate School of Life Sciences, Tohoku University, Sendai, Japan
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Yi Luo
1Graduate School of Life Sciences, Tohoku University, Sendai, Japan
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Hidemasa Suzuki
1Graduate School of Life Sciences, Tohoku University, Sendai, Japan
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Hiromu Kameoka
1Graduate School of Life Sciences, Tohoku University, Sendai, Japan
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Cyril Libourel
2LRSV, Université de Toulouse, CNRS, UPS, Toulouse INP, Auzeville-Tolosane, France
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Jean Keller
2LRSV, Université de Toulouse, CNRS, UPS, Toulouse INP, Auzeville-Tolosane, France
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Keiko Sakakibara
6Department of Life Science, Rikkyo University, Tokyo, Japan
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Tomoaki Nishiyama
7Research Center for Experimental Modeling of Human Disease, Kanazawa University, Kanazawa, Japan
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Tomomi Nakagawa
8National Institute for Basic Biology, Okazaki, Japan
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Kiyoshi Mashiguchi
9Institute for Chemical Research, Kyoto University, Kyoto, Japan
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Kenichi Uchida
10Department of Biosciences, Teikyo University, Tochigi, Japan
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Kaori Yoneyama
11Graduate School of Agriculture, Ehime University, Ehime, Japan
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Yoshikazu Tanaka
1Graduate School of Life Sciences, Tohoku University, Sendai, Japan
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Shinjiro Yamaguchi
9Institute for Chemical Research, Kyoto University, Kyoto, Japan
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Masaki Shimamura
12Graduate School of Integrated Sciences for Life, Hiroshima University, Hiroshima, Japan
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Pierre-Marc Delaux
2LRSV, Université de Toulouse, CNRS, UPS, Toulouse INP, Auzeville-Tolosane, France
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  • ORCID record for Pierre-Marc Delaux
  • For correspondence: junko.kyozuka.e4@tohoku.ac.jp tnomura@cc.utsunomiya-u.ac.jp pierre-marc.delaux@lrsv.ups-tlse.fr
Takahito Nomura
3United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Tokyo, Japan
4Center for Bioscience Research and Education, Utsunomiya University, Tochigi, Japan
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  • ORCID record for Takahito Nomura
  • For correspondence: junko.kyozuka.e4@tohoku.ac.jp tnomura@cc.utsunomiya-u.ac.jp pierre-marc.delaux@lrsv.ups-tlse.fr
Junko Kyozuka
1Graduate School of Life Sciences, Tohoku University, Sendai, Japan
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  • For correspondence: junko.kyozuka.e4@tohoku.ac.jp tnomura@cc.utsunomiya-u.ac.jp pierre-marc.delaux@lrsv.ups-tlse.fr
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Abstract

In flowering plants, carotenoid-derived strigolactones (SLs) have dual functions as hormones that regulate growth and development, and as rhizosphere signaling molecules that induce symbiosis with arbuscular mycorrhizal (AM) fungi. Here, we report the identification of bryosymbiol (BSB), a previously unidentified SL from the bryophyte Marchantia paleacea. BSB is also found in vascular plants, indicating that it is ancestral in land plants. BSB synthesis is enhanced at AM symbiosis permissive conditions and BSB deficient mutants are impaired in AM symbiosis. In contrast, the absence of BSB synthesis has little effect on the growth and gene expression. We show that the introduction of the SL receptor of Arabidopsis renders M. paleacea cells BSB-responsive. These results suggest that BSB is not perceived by M. paleacea cells due to the lack of cognate SL receptors. We propose that SLs originated as AM symbiosis-inducing rhizosphere signaling molecules and were later recruited as plant hormone.

Competing Interest Statement

The authors have declared no competing interest.

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An Ancestral Function of Strigolactones as Symbiotic Rhizosphere Signals
Kyoichi Kodama, Mélanie K. Rich, Akiyoshi Yoda, Shota Shimazaki, Xiaonan Xie, Kohki Akiyama, Yohei Mizuno, Aino Komatsu, Yi Luo, Hidemasa Suzuki, Hiromu Kameoka, Cyril Libourel, Jean Keller, Keiko Sakakibara, Tomoaki Nishiyama, Tomomi Nakagawa, Kiyoshi Mashiguchi, Kenichi Uchida, Kaori Yoneyama, Yoshikazu Tanaka, Shinjiro Yamaguchi, Masaki Shimamura, Pierre-Marc Delaux, Takahito Nomura, Junko Kyozuka
bioRxiv 2021.08.20.457034; doi: https://doi.org/10.1101/2021.08.20.457034
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An Ancestral Function of Strigolactones as Symbiotic Rhizosphere Signals
Kyoichi Kodama, Mélanie K. Rich, Akiyoshi Yoda, Shota Shimazaki, Xiaonan Xie, Kohki Akiyama, Yohei Mizuno, Aino Komatsu, Yi Luo, Hidemasa Suzuki, Hiromu Kameoka, Cyril Libourel, Jean Keller, Keiko Sakakibara, Tomoaki Nishiyama, Tomomi Nakagawa, Kiyoshi Mashiguchi, Kenichi Uchida, Kaori Yoneyama, Yoshikazu Tanaka, Shinjiro Yamaguchi, Masaki Shimamura, Pierre-Marc Delaux, Takahito Nomura, Junko Kyozuka
bioRxiv 2021.08.20.457034; doi: https://doi.org/10.1101/2021.08.20.457034

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