CAREER: How SFR2 allows chloroplast envelope membranes to survive freezing, from initial signal to molecular mechanism.

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Weather instability is predicted to be on the rise and it threatens crop yields. Specifically, out-of-season frosts damage crops costing billions of dollars annually, and restricting growing seasons to avoid potential frosts likely costs in the tens of billions. Also important, the global population is expected to rise and the need to grow more crops on the same land is immediate. Poor understanding of freezing tolerance mechanisms constrains development of more tolerant crops. This project will ultimately provide new knowledge that can guide strategies to engineer freezing tolerance in crop plants. An enzyme named "Sensitive to Freezing 2" (SFR2) is known to help plants survive freezing by changing the building blocks of chloroplast membranes. Although SFR2's action is known, the way that SFR2 is activated to respond to freezing conditions and the way that its actions provide an advantage are only hypothesized. This project tests the hypotheses using a unique blend of genetics, biochemistry, and biophysical approaches. It is expected that the results will immediately enhance efforts to generate cold-tolerant crops and will also impact research on membrane temperature stability in other species and engineering systems. Throughout the project, training of Nebraskan post-doctoral researchers and graduate students in plant science will be improved to include public communication and other convergent skillsets. In doing so, members of the general public in Nebraska will also benefit.An enzyme known as Sensitive to Freezing 2 (SFR2) remodels the chloroplast envelope membranes by reducing monogalactolipids and increasing oligogalactolipids. Plants expressing catalytically inactive point mutants of SFR2 are more susceptible to freezing than wildtype plants. Recent evidence from the investigator's lab indicates that SFR2 is activated during freezing by cytoplasmic acidification. Acidification of the cytoplasm also occurs during other stresses in which SFR2 is not active. This and other data suggest that SFR2 activity is tied to a more global cellular response to freezing temperatures in which it directly stabilizes the chloroplast envelope membranes by altering their physical properties. This project will test this hypothesis through the following objectives: (1) Define how membrane stability is affected by SFR2-dependent changes to lipids. (2) Determine if SFR2 activity is repressed by post-translational modification. (3) Define the diversity of chloroplast envelope membrane freezing stabilization mechanisms. These objectives identify mechanisms allowing membrane integrity during freezing temperatures and define how they work (Obj. 1, Obj. 3), and they define a critical cellular freezing signal (Obj. 2). Finally, they will also provide a comprehensive understanding of chloroplast envelope stabilization mechanisms useful in multiple fields. The following training and science literacy objectives are integrated with the above research: (4) Provide comprehensive training for next-generation scientists to be effective researchers and communicators. (5) Educate and engage the public on the societal impact of plant science with innovative graphic novels and interactive presentations.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.