MIRO-mediated mitochondrial fusion is required for stomatal immunity in Arabidopsis

Pengfei Lu, Jiejie Li
Beijing Key Laboratory of Gene Resource and Molecular Development, College of Life Science, Beijing Normal University, Beijing, 100875, China ; Key Laboratory of Cell Proliferation and Regulation of Ministry of Education, College of Life Science, Beijing Normal University, Beijing, 100875, China

Mitochondria are dynamic organelles that constantly undergo cycles of fusion and fission. The balance between these processes is critical for maintaining mitochondrial homeostasis. In our current study, we report a previously undescribed phenomenon: upon activation of innate immunity, mitochondrial morphology in guard cells remodels from short rod-shaped to elongated linear structures. Disruption of these morphological changes results in compromised stomatal closure induced by the bacterial elicitor flg22. We further identified that MIRO1, a mitochondrial outer membrane GTPase, is highly expressed in guard cells and exhibits significantly elevated transcription levels upon flg22 stimulation. Mutations in MIRO1 lead to compromised stomatal closure triggered by flg22 and enhanced susceptibility to bacterial infection. Further investigations revealed that MIRO1 is a physiological substrate of two pathogen-responsive mitogen-activated protein kinases, MPK3 and MPK6. This phosphorylation modification triggers MIRO1 oligomerization and upregulates its GTPase activity. The oligomerized MIRO1 is enriched at the contact interface of two closely positioned mitochondria, facilitating mitochondrial fusion. The MIRO1-mediated mitochondrial elongation is required for mitochondrial quality control and the subsequent metabolic conversion of osmotically active molecules for stomatal closure. Taken together, our investigation uncovers the biological significance and underlying molecular mechanisms of mitochondrial remodeling during stomatal immunity.