Warming triggers stomatal opening by enhancement of photosynthesis and ensuing guard cell CO2 sensing, whereas higher temperatures induce a photosynthesis‐uncoupled response

• Published in: The New phytologist 2024-12, Vol.244 (5), p.1847-1863
• Main Authors: Pankasem, Nattiwong, Hsu, Po‐Kai, Lopez, Bryn N. K., Franks, Peter J., Schroeder, Julian I.
• Format: Article
• Language: English
• Subjects: Abscisic acid; Air temperature; Biosynthesis; blue light; Carbon dioxide; Cell signaling; Environmental effects; Flowering; guard cell; heat; Heat stress; Heat tolerance; High temperature; Leaves; Mutants; Photoreceptors; Photosynthesis; Phytochrome B; Plant layout; Plants (botany); protein kinase; Signal transduction; Stomata; Stress functions; Temperature; Temperature effects; Vapor pressure; Vapour pressure; Water loss
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.20121

Summary Plants integrate environmental stimuli to optimize photosynthesis vs water loss by controlling stomatal apertures. However, stomatal responses to temperature elevation and the underlying molecular genetic mechanisms remain less studied. We developed an approach for clamping leaf‐to‐air vapor pressure difference (VPDleaf) to fixed values, and recorded robust reversible warming‐induced stomatal opening in intact plants. We analyzed stomatal temperature responses of mutants impaired in guard cell signaling pathways for blue light, abscisic acid (ABA), CO2, and the temperature‐sensitive proteins, Phytochrome B (phyB) and EARLY‐FLOWERING‐3 (ELF3). We confirmed that phot1‐5/phot2‐1 leaves lacking blue‐light photoreceptors showed partially reduced warming‐induced stomatal opening. Furthermore, ABA‐biosynthesis, phyB, and ELF3 were not essential for the stomatal warming response. Strikingly, Arabidopsis (dicot) and Brachypodium distachyon (monocot) mutants lacking guard cell CO2 sensors and signaling mechanisms, including ht1, mpk12/mpk4‐gc, and cbc1/cbc2 abolished the stomatal warming response, suggesting a conserved mechanism across diverse plant lineages. Moreover, warming rapidly stimulated photosynthesis, resulting in a reduction in intercellular (CO2). Interestingly, further enhancing heat stress caused stomatal opening uncoupled from photosynthesis. We provide genetic and physiological evidence that the stomatal warming response is triggered by increased CO2 assimilation and stomatal CO2 sensing. Additionally, increasing heat stress functions via a distinct photosynthesis‐uncoupled stomatal opening pathway.