Collaborative Research: NSF-BSF: Under Pressure: The evolution of guard cell turgor and the rise of the angiosperms

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Stomata are the pores on the surface of leaves through which the CO2 needed for photosynthesis enters. At the same time, stomata are also the main way that plants lose water to the atmosphere. Balancing the ratio of CO2 gained and water lost from leaves is essential for plant survival because unregulated water loss would lead to rapid desiccation and death. Stomata open by increasing the internal turgor pressure of paired “guard” cells, which causes the cells to bow apart creating a hole or pore, and close by reducing guard cell turgor pressure. Despite the key role of turgor pressure in stomatal functioning, progress has been limited by the lack of a method to measure turgor pressures in photosynthesizing leaves. This project introduces a new approach to determine guard cell turgor pressure in which a laser is used to trigger the formation of a gas bubble inside a cell, and the size and speed by which this bubble is pushed back into solution due to the turgor pressure is recorded. This method will be used to quantify the range of guard cell turgor pressure across vascular plants and to elucidate the regulation of stomatal opening and closing in response to environmental stresses such as drought and heatwaves. The research will advance understanding of controls on the productivity and resiliency of terrestrial ecosystems, including agricultural systems important to the U.S. bioeconomy and food security, and provide insights into the evolution of stomatal regulation across diverse plant lineages. The project includes educational and outreach activities with the Harvard Museum of Natural History and the Purdue Agriculture Traveling Exhibit that will reach large public audiences and students from K-12 levels. Training in modern scientific research using state of the art equipment and techniques will include postdoctoral fellows, graduate students, and undergraduate students. Immersive laboratory experiences in summer programs and the development of hands-on demonstrations and teaching modules for multiple grade levels will also be undertaken. The coordinated evolution of increased leaf vascular system efficiency with both a reduction in stomatal size and increase in stomatal number is believed to be one of the critical components of angiosperm dominance since the Cretaceous. Yet, controlling more stomata of smaller size likely imposed new constraints in realizing potential photosynthetic gains conferred by more efficient hydraulics. Using a newly developed method that enables for the first-time direct measurement of guard cell and epidermal cell turgor in situ, the research team will determine if angiosperms maintain higher guard cell turgor, enabling their higher rates of photosynthesis and altering stomatal dynamics and control. These results will be compared to ferns, lycophytes and gymnosperms that have stomata that do not interact mechanically with epidermal cells and used to establish clear and definitive links between guard cell anatomy, hormonal signaling, interaction between adjacent epidermal cells, and hydraulics, all of which have eluded scientists for decades because of a lack of direct leaf cell turgor measurements. The results will reveal fundamental biophysical and physiochemical principles of guard cell control in determining the rate of maximum photosynthesis, but also sensitivity to the environment in response to drought and the protection of the leaf vascular network from hydraulic failure. This will enable the development of a more comprehensive understanding of stomatal biology and leaf physiology, both over evolutionary time but also in response to a rapidly changing climate. Outreach and educational efforts for K-12 and undergraduate students will be conducted in collaboration with the Harvard Museum of Natural History and the Purdue Agriculture Traveling Exhibit. Training in modern scientific research using state of the art equipment and techniques will include postdoctoral fellows and graduate students in a long-running training program in physiological ecology. This project also involves international partnerships via the US-Israel Binational Foundation.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.