ERA-CAPS: Mechano-purino signaling in abiotic stress

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To survive, plants must maintain an upright stem in the face of wind, while their roots must forage for water and nutrients despite soil hardness and compaction. Wind induces adaptive, structural changes in stems, such as secondary thickening. Roots penetrate hard substrate and modify their growth and architecture as obstacles are sensed. Despite this ability to adapt, mechanical stresses contribute significantly to annual crop loss and decreased yield, problems likely to worsen with changing climate and increasingly stormy and erratic weather. Therefore, identifying the components of mechano-sensing and signaling is a priority for crop improvement. This project explores the role of adenosine triphosphate (ATP), generally known as an intracellular energy source, as an extracellular signal in response to mechanical stress (e.g., wind). The three groups involved have specific expertise in studies of plant signaling, especially related to extracellular ATP, as well as studies of how plants respond to mechanical stress. This project is relevant and timely regarding sustainable agricultural; better adapted crop plants are needed urgently but there is little information on how plants withstand mechanical stress. The research will identify new components of how stems and roots respond to wind and soil hardness, respectively, helping crop improvement programs for lodging, wind resistance and penetrative root growth. In addition to aiding water and nutrient uptake, deeper roots with more lateral outgrowth improve soil structure, thus improving water and nutrient retention. Wind damage also inflicts losses on forestry and urban landscapes. This project will provide foundational understanding on the adaptability of plants to mechanical stress and for improving crop yield for the increasing global population. Recent evidence points to an intersection between mechanobiology and purinergic signaling in plants. Purinergic signaling is the transduction of signals elicited by extracellular purine nucleotides, such as ATP. Specifically, extracellular ATP (eATP) has been found to increase as cells expand (a process that generates intrinsic mechanical stress) and eATP also increases in response to extrinsic mechanical stress. Moreover, eATP affects root development and governs the transcriptional response to wounding as the most severe mechanical stress. The recently discovered plant purino receptor, Arabidopsis DORN1, provides a unique opportunity to explore at the molecular and whole plant levels the relationships between purino- and mechano-signalling. Critically, the structure of DORN1 indicates it serves as a reporter of cell wall state. In this project, two, cross-disciplinary purino-signalling groups (Stacey and Davies) and a mechanobiology group (Moulia) will delineate the DORN1 mechano-purino signaling system using molecular, biochemical and biophysical approaches. Structure-function relationships of DORN1 will be probed to determine how its attachment to the wall can regulate its eATP binding activity. The cell membrane Ca2+ channels mediating the DORN1-dependent Ca2+ increase in roots and stems will be characterized. Phenotyping mutants will determine the impact of DORN1 and downstream Ca2+ channels on stem posture control, adaptive response to wind, root Ca2+ response and mechano-regulated growth. Outcomes of the research is important to agriculture and society because the results obtained in Arabidopsis can be translated to crops. Understanding how plant walls cope with mechanical stresses will provide a platform to overcome crop lodging and increasing crop resilience to environmental challenges. Combined with training students in interdisciplinary science, the project outcomes will contribute to food and national security.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.