A non-canonical BZR/BES transcription factor regulates the development of haploid reproductive organs in Marchantia polymorpha

Tomoyuki Furuya; Natsumi Saegusa; Shohei Yamaoka; Yuki Tomoita; Naoki Minamino; Masaki Niwa; Keisuke Inoue; Chiaki Yamamoto; Kazuki Motomura; Shunji Shimadzu; Ryuichi Nishihama; Kimitsune Ishizaki; Takashi Ueda; Hidehiro Fukaki; Takayuki Kohchi; Hiroo Fukuda; Masahiro Kasahara; Takashi Araki; Yuki Kondo

doi:10.1038/s41477-024-01669-0

A non-canonical BZR/BES transcription factor regulates the development of haploid reproductive organs in Marchantia polymorpha

Nat Plants. 2024 Apr 11. doi: 10.1038/s41477-024-01669-0. Online ahead of print.

Authors

Tomoyuki Furuya^{1

2

3}, Natsumi Saegusa⁴, Shohei Yamaoka⁴, Yuki Tomoita⁴, Naoki Minamino^{5

6}, Masaki Niwa^{4

7}, Keisuke Inoue⁴, Chiaki Yamamoto⁸, Kazuki Motomura^{8

9}, Shunji Shimadzu^{10

11}, Ryuichi Nishihama^{4

12}, Kimitsune Ishizaki¹⁰, Takashi Ueda^{5

13}, Hidehiro Fukaki¹⁰, Takayuki Kohchi⁴, Hiroo Fukuda^{11

14

15}, Masahiro Kasahara⁸, Takashi Araki⁴, Yuki Kondo^{16

17

18}

Affiliations

¹ College of Life Sciences, Ritsumeikan University, Kusatsu, Japan. furu@fc.ritsumei.ac.jp.
² Graduate School of Science, Kobe University, Kobe, Japan. furu@fc.ritsumei.ac.jp.
³ Graduate School of Science, The University of Tokyo, Tokyo, Japan. furu@fc.ritsumei.ac.jp.
⁴ Graduate School of Biostudies, Kyoto University, Kyoto, Japan.
⁵ Division of Cellular Dynamics, National Institute for Basic Biology, Okazaki, Japan.
⁶ Graduate School of Science and Technology, Kumamoto University, Kumamoto, Japan.
⁷ GRA&GREEN Inc., Nagoya, Japan.
⁸ College of Life Sciences, Ritsumeikan University, Kusatsu, Japan.
⁹ Japanese Science and Technology Agency, PRESTO, Kawaguchi, Japan.
¹⁰ Graduate School of Science, Kobe University, Kobe, Japan.
¹¹ Graduate School of Science, The University of Tokyo, Tokyo, Japan.
¹² Faculty of Science and Technology, Tokyo University of Science, Noda, Japan.
¹³ Basic Biology Program, Graduate Institute for Advanced Studies, SOKENDAI, Okazaki, Japan.
¹⁴ Faculty of Bioenvironmental Science, Kyoto University of Advanced Science, Kameoka, Japan.
¹⁵ Akita Prefectural University, Akita, Japan.
¹⁶ Graduate School of Science, Kobe University, Kobe, Japan. kondo.yuki.sci@osaka-u.ac.jp.
¹⁷ Graduate School of Science, The University of Tokyo, Tokyo, Japan. kondo.yuki.sci@osaka-u.ac.jp.
¹⁸ Department of Biological Sciences, Graduate School of Science, Osaka University, Toyonaka, Japan. kondo.yuki.sci@osaka-u.ac.jp.

PMID: 38605238
DOI: 10.1038/s41477-024-01669-0

Abstract

Gametogenesis, which is essential to the sexual reproductive system, has drastically changed during plant evolution. Bryophytes, lycophytes and ferns develop reproductive organs called gametangia-antheridia and archegonia for sperm and egg production, respectively. However, the molecular mechanism of early gametangium development remains unclear. Here we identified a 'non-canonical' type of BZR/BES transcription factor, MpBZR3, as a regulator of gametangium development in a model bryophyte, Marchantia polymorpha. Interestingly, overexpression of MpBZR3 induced ectopic gametangia. Genetic analysis revealed that MpBZR3 promotes the early phase of antheridium development in male plants. By contrast, MpBZR3 is required for the late phase of archegonium development in female plants. We demonstrate that MpBZR3 is necessary for the successful development of both antheridia and archegonia but functions in a different manner between the two sexes. Together, the functional specialization of this 'non-canonical' type of BZR/BES member may have contributed to the evolution of reproductive systems.

Abstract

Grants and funding