As temperatures rise, researchers identify mechanisms behind plant response to warming

Microscopic pores on the surface of leaves called stomata help plants “breathe” by controlling how much water they lose to evaporation. These stomatal pores also enable and control carbon dioxide intake for photosynthesis and growth.

As far back as the 19^th century, scientists have known that plants increase their stomatal pore openings to transpire, or “sweat,” by sending water vapor through stomata to cool off. Today, with global temperatures and heat waves on the rise, widening stomatal pores are considered a key mechanism that can minimize heat damage to plants.

But for more than a century, plant biologists have lacked a full accounting of the genetic and molecular mechanisms behind increased stomatal “breathing” and transpiration processes in response to elevated temperatures.

University of California San Diego School of Biological Sciences PhD student Nattiwong Pankasem and Professor Julian Schroeder have constructed a detailed picture of these mechanisms. Their findings, published in the journal New Phytologist, identify two paths that plants use to handle rising temperatures.

“With increasing global temperatures, there’s obviously a threat to agriculture with the impact of heat waves,” said Schroeder. “This research describes the discovery that rising temperatures cause stomatal opening by one genetic pathway (mechanism), but if the heat steps up even further, then there’s another mechanism that kicks in to increase stomatal opening.”

For decades, scientists struggled to find a clear method to decipher the mechanisms underlying rising temperature-mediated stomatal openings due to the intricate measurement processes required. The difficulty is rooted in the complex mechanics involved in setting air humidity (also known as the vapor pressure difference, or VPD) to constant values while the temperature increases, and the trickiness of picking apart temperature and humidity responses.

Pankasem helped solve this problem by developing a novel approach for clamping the VPD of leaves to fixed values under increasing temperatures. He then teased out the genetic mechanisms of a range of stomatal temperature responses, including factors such as blue-light sensors, drought hormones, carbon dioxide sensors and temperature-sensitive proteins.

Important for this research was a new generation gas exchange analyzer that allows improved control of the VPD (clamping the VPD to fixed values). Researchers can now conduct experiments that elucidate the temperature effects on stomatal opening without the need to remove leaves from whole living plants.

The results revealed that the stomatal warming response is dictated by a mechanism found across plant lineages. In this study, Pankasem investigated the genetic mechanisms of two plant species, Arabidopsis thaliana, a well-studied weed species and Brachypodium distachyon, a flowering plant that is related to major grain crops such as wheat, maize and rice, representing an opportune model for these crops.

The researchers found that carbon dioxide sensors are a central player in the stomatal warming-cooling responses. Carbon dioxide sensors detect when leaves undergo rapid warming. This starts an increase in photosynthesis in the warming leaves, which results in a reduction in carbon dioxide. This then initiates the stomatal pores to open, allowing plants to benefit from the increase in carbon dioxide intake.

Interestingly, the study also found a second heat response pathway. Under extreme heat, photosynthesis in plants is stressed and declines and the stomatal heat response was found to bypass the carbon dioxide sensor system and disconnect from normal photosynthesis-driven responses. Instead, the stomata employ a second heat response pathway, not unlike gaining entry through a backdoor to a house, to “sweat” as a cooling mechanism.

“The impact of the second mechanism, in which plants open their stomata without gaining benefits from photosynthesis would result in a reduction in water use efficiency of crop plants,” said Pankasem. “Based on our study, plants are likely to demand more water per unit of CO₂ taken in. This may have direct implications on irrigation planning for crop production and large-scale effects of increased transpiration of plants in ecosystems on the hydrological cycle in response to global warming.”

“This work shows the importance of curiosity-driven, fundamental research in helping to address societal challenges, build resiliency in key areas like agriculture, and, potentially, advance the bioeconomy,” said Richard Cyr, a program director in the U.S. National Science Foundation Directorate for Biological Sciences, which partially funded the research. “Further understanding of the molecular complexities that control the basis of stomatal function at higher temperatures could lead to strategies to limit the amount of water needed for farming in the face of global increases in temperature.”

With the new details in hand, Pankasem and Schroeder are now working to understand the molecular and genetic mechanisms behind the secondary heat response system.

The coauthors of the study are: Nattiwong Pankasem, Po-Kai Hsu, Bryn Lopez, Peter Franks and Julian Schroeder. The research was funded by the Human Frontier Science Program (RGP0016/2020) and the National Science Foundation (MCB 2401310).