Apoplastic metabolomics reveals sugars as mesophyll messengers regulating guard cell ion transport under red light
Guard cell pairs in the leaf epidermis enclose stomata, microscopic pores mediating CO<sub>2</sub> uptake and water loss. Historical data suggest that signals from interior mesophyll tissue may modulate guard-cell regulation of stomatal apertures, but the molecular identity of any metabolite-based signals has remained elusive. We discovered that extracellular (apoplastic) fluid from Arabidopsis thaliana and Vicia faba enhances red-light-induced stomatal opening. Our extensive metabolomics analyses identified 448 apoplastic metabolites; among these, both sugars (photosynthetic products) and maleic acid increased under red light and caused enhanced stomatal opening. Immunohistochemical assays demonstrated sucrose upregulation of H<sup>+</sup>-ATPase phosphorylation, indicating increased ATPase activity. Patch clamp assays revealed that sucrose inhibits slow anion currents, thus opposing anion efflux. These impacts occurred at sucrose concentrations matching those present endogenously under red light. These regulatory influences promote guard-cell solute import and retention, which drive stomatal opening. Our research thus addresses the decades-long question concerning the existence, identity and mechanistic impact of mesophyll messengers that coordinate photosynthesis with stomatal response.
Authors
- Sunheng Yon (ORCID: https://orcid.org/0009-0006-0060-0139)
- Mami Okamoto
- Timothy Jegla (ORCID: https://orcid.org/0000-0001-8616-2390)
- Adi Yaaran (ORCID: https://orcid.org/0000-0001-9343-9976)
- Yotam Zait (ORCID: https://orcid.org/0000-0003-4266-1635)
- Mengmeng Zhu (ORCID: https://orcid.org/0000-0002-5161-813X)
- Masami Yokota Hirai (ORCID: https://orcid.org/0000-0003-0802-6208)
- Yunqing Zhou (ORCID: https://orcid.org/0000-0002-2808-4192)
- Sarah M. Assmann (ORCID: https://orcid.org/0000-0003-4541-1594)
- Toshinori Kinoshita (ORCID: https://orcid.org/0000-0001-7621-1259)
- Eigo Ando (ORCID: https://orcid.org/0000-0001-6232-6573)
- Sixue Chen (ORCID: https://orcid.org/0000-0002-6690-7612)
- Yuki Hayashi
Institutions
- Pennsylvania State University (US)
- National Agriculture and Food Research Organization (JP)
- Hebrew University of Jerusalem (IL)
- University of Mississippi (US)
- RIKEN Center for Sustainable Resource Science (JP)
- Institute of Vegetable and Floriculture Science (JP)
- Nagoya University (JP)
- The University of Tokyo (JP)
Publication Details
- Journal
- Nature Plants
- Published
- 2025-08-25
- DOI
- https://doi.org/10.1038/s41477-025-02078-7
- Citations
- 9
- Primary Topic
- Light effects on plants
- Type
- article
- Field-Weighted Citation Impact
- 15.75
Funders
- National Science Foundation
- U.S. Department of Agriculture
- University of Pennsylvania
- Pennsylvania State University
- Cabinet Office, Government of Japan
- Israel Science Foundation
- University of Tokyo
- National Institutes of Health
- National Institute of Food and Agriculture
- University of California, Davis
- Japan Society for the Promotion of Science
- Bio-oriented Technology Research Advancement Institution
- Division of Molecular and Cellular Biosciences
- Division of Integrative Organismal Systems