Co-option and neofunctionalization of stomatal executors for defence against herbivores in Brassicales
Co-option of gene regulatory networks leads to the acquisition of new cell types and tissues. Stomata, valves formed by guard cells (GCs), are present in most land plants and regulate CO<sub>2</sub> exchange. The transcription factor (TF) FAMA globally regulates GC differentiation. In the Brassicales, FAMA also promotes the development of idioblast myrosin cells (MCs), another type of specialized cell along the vasculature essential for Brassicales-specific chemical defences. Here we show that in Arabidopsis thaliana, FAMA directly induces the TF gene WASABI MAKER (WSB), which triggers MC differentiation. WSB and STOMATAL CARPENTER 1 (SCAP1, a stomatal lineage-specific direct FAMA target), synergistically promote GC differentiation. wsb mutants lacked MCs and the wsb scap1 double mutant lacked normal GCs. Evolutionary analyses revealed that WSB is conserved across stomatous angiosperms. We propose that the conserved and reduced transcriptional FAMA-WSB module was co-opted before evolving to induce MC differentiation.
Authors
- Yasunori Ichihashi (ORCID: https://orcid.org/0000-0003-1935-4397)
- Kie Kumaishi
- Nobutoshi Yamaguchi (ORCID: https://orcid.org/0000-0003-3738-6157)
- Kyoko Sunuma
- Takamasa Suzuki (ORCID: https://orcid.org/0000-0002-1977-0510)
- Mayu Sagara
- Atsushi Takemiya (ORCID: https://orcid.org/0000-0003-2642-6758)
- Takuya Iwami
- Shigeo S. Sugano (ORCID: https://orcid.org/0000-0001-9986-2839)
- Mai Tanida
- Takayuki Kohchi (ORCID: https://orcid.org/0000-0002-9712-4872)
- Keita Horiuchi
- Toshiro Ito (ORCID: https://orcid.org/0000-0002-8206-2787)
- Mutsumi Watanabe (ORCID: https://orcid.org/0000-0001-9792-2615)
- Makoto Shirakawa (ORCID: https://orcid.org/0000-0003-3719-7081)
- Shohei Yamaoka (ORCID: https://orcid.org/0000-0003-4154-9967)
- Takayuki Tohge (ORCID: https://orcid.org/0000-0001-5555-5650)
- Tatsuyoshi Nakanishi
- S. Yoshida
- Tomoki Oguro
Institutions
- Yamaguchi University (JP)
- Chubu University (JP)
- Kyoto University (JP)
- Japan Science and Technology Agency (JP)
- RIKEN BioResource Research Center (JP)
- National Institute of Advanced Industrial Science and Technology (JP)
- Nara Institute of Science and Technology (JP)
Publication Details
- Journal
- Nature Plants
- Published
- 2025-02-24
- DOI
- https://doi.org/10.1038/s41477-025-01921-1
- Citations
- 7
- Primary Topic
- Photosynthetic Processes and Mechanisms
- Type
- article
- Field-Weighted Citation Impact
- 5.64
Funders
- Japan Society for the Promotion of Science
- Core Research for Evolutional Science and Technology
- Precursory Research for Embryonic Science and Technology