Intellectual Merit: 

Stomatal pores in plants are formed by pairs of guard cells. Thousands such small adjustable stomatal pores are found in the epidermis of all plant leaves. Stomata regulate the diffusion of carbon dioxide (CO₂) into leaves for photosynthetic carbon fixation that is required for plant growth. At the same time stomatal pores control over 90 % of water loss by plants. A network of signal transduction mechanisms sense and transduce CO₂ concentration changes to regulate stomatal apertures for optimization of CO₂ influx, water loss and plant growth under diverse conditions. Photosynthesis and respiration cause large daily CO₂ concentration (C_i) changes in the airspaces inside leaves. Moreover, atmospheric [CO₂] is predicted to double during this century and this continuing [CO₂] rise reduces stomatal pore apertures of plants. This will have profound effects on global gas exchange, water use efficiency of plants and heat stress resistance of plants.

In this NSF-Funded project we have discovered key cellular, molecular, genetic and biophysical signaling mechanisms that mediate CO₂ control of stomatal conductance and water loss by plants. This project investigated new models and identified the elusive primary CO₂/bicarbonate sensor in guard cells that controls plant CO₂ intake and water loss.

The CO₂ and/or bicarbonate sensors that control stomatal movements remained unknown. The continuing rise in the atmospheric carbon dioxide (CO2) concentration causes stomatal closing, thus critically affecting transpirational water loss, photosynthesis and plant growth. Within this research project we discovered the long sought primary stomatal CO₂ sensor. We discovered that elevated CO₂ triggers an interaction of MAP kinases (MPK4 and MPK12) with the High Temperature 1 (HT1) protein kinase, thus inhibiting HT1 protein kinase activity. At low CO₂, HT1 phosphorylates and activates the downstream CBC1 kinase, which in turn signals stomata to open. The CO₂ sensor consisting of the high CO₂/bicarbonate-induced interaction of MPK4/12 and HT1, could be explained by a structural AlphaFold2- and Gaussian-accelerated dynamics-generated model. Unexpectedly, we further found that MAP kinase activity is not required for CO₂ sensor function and for CO₂-triggered HT1 inhibition and stomatal closing. Our findings revealed that MPK4/12 and HT1 together constitute the long-sought primary stomatal CO₂/bicarbonate sensor.

We examined how the guard cell epigenome responds to changes in CO₂ concentrations. We discovered that CO₂ elevation surprisingly causes only minimal changes in chromatin structure. Our research demonstrated that these CO₂ responses are substantially less dependent on chromatin remodeling than drought-linked responses. This correlates with the quick reversibility of CO₂ responses, enabling rapid adjustment of instantaneous water use efficiency of plants when light conditions change (such as cloud cover, shading and night time). In contrast, stomatal drought responses can take several days to reverse.

Our research further demonstrated an unexpected convergence mechanism by which CO₂ signal transduction merges with the drought stress-triggered pathway that mediates control of stomatal movements. This research indicates that the stomatal CO₂ response can, in first order, be bred or engineered to optimize plant growth while reducing interference with the drought response.

Several additional important advances were made in identifying and characterizing new CO₂ signal transduction mechanisms that have enhanced our understanding of this important response and we published reviews on this area of present interest.

In summary, this research has provided discovery of genes, mechanisms and the long sought primary CO₂ sensor for future elucidation of the CO₂ signal transduction network by which the presently continuing increase in atmospheric CO₂ concentration will affect plant gas exchange between plants and the environment.

Broader Impacts:

This research project has strong potential for providing new tools for adapting plants to the continuing rise in the atmospheric CO₂ concentration, limited water availability, droughts and heat stress, including in light of extreme weather events. Our research advances are also relevant for exploring optimized plant and tree growth and productivity in regions of sufficient water and soil nutrients, given the increasing atmospheric CO₂ fertilization. Determining the molecular and cellular and network mechanisms by which CO₂ regulates stomatal conductance is fundamental to understanding the regulation of gas exchange between plants and the atmosphere and will help predict effects of atmospheric CO₂ elevation on crop plants and plant carbon sinks. UCSD has submitted patent applications on aspects of these research advances.

We pursued outreach efforts through research training, internships and preparation of under-represented undergraduate and high school students. Furthermore, the PI gave presentations to school students, trained disadvantaged high school students and undergraduate students in independent research projects, and worked to offer and expand high school student university internship offerings. The PI prepared a paper with undergraduate students for the public on the subject of the impacts of heat waves and rising CO₂ on crop resilience and food security. In addition, both PIs trained and prepared postdoctoral, graduate and undergraduate students to prepare the next generation for advanced independent careers in industry, technology, research and science education.

Last Modified: 11/29/2024
Modified by: Julian I Schroeder