Genetic and physiological mechanisms of a fitness trade-off across environments

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Organisms in temperate zones, when exposed to cool autumn temperatures, undergo cellular and metabolic changes which increase survival through freezing. These responses are likely to be energetically costly, requiring appropriate adjustments for conditions days to months in the future. Too little will not prepare for freezing, too much may inhibit growth and reproduction. The trade-off between the costs and benefits of adaptation to seasonality can limit where native species and crops can thrive. Climatic variability threatens the capacities of organisms to “predict” the future environment and will contribute to extinction risks for native species and reduced crop production. Yet, we do not know how most organisms acclimate for winter, and even less about the costs of such acclimation. The proposed research will, for the first time, connect our understanding of adaptation and trade-offs from genes and metabolism to performance in contrasting natural environments. The study system has a foundation of over a decade of field experimental and climate data, and both natural and engineered variants of a gene that regulates cold acclimation and is hypothesized to underlie differences in survival and reproduction across contrasting climates. This focal regulatory gene responds to cold in many plant species, and the costs of acclimation are directly important for climate resilience of native species and for improving agronomical varieties. Broader impact activities for middle and high school students on organismal responses to climate change will be developed, including a “Data Nugget” module to promote students’ quantitative skills by answering scientific questions using real data. Fitness trade-offs across environments are key drivers of biological diversification. The ultimate, but yet unrealized, goal in understanding the genetic basis of fitness trade-offs is to identify the full causal chain connecting naturally occurring sequence polymorphisms, molecular and organismal phenotypes, and fitness in the contrasting environments in which the organisms evolved. The proposed work uses locally adapted ecotypes of Arabidopsis thaliana from Italy and Sweden, for which cold-acclimated freezing tolerance loci are hypothesized to underlie genetic trade-offs. A naturally occurring polymorphism in a transcription factor encoding gene CBF2 was identified as responsible for a major freezing tolerance locus. The proposed experiments will test the hypothesis that CBF2 mediates a genetic trade-off across environments, and determine the genetic and metabolic mechanisms by which this occurs. Genetic stocks include Near Isogenic and mutant lines in multiple ecotypic backgrounds that contain, or mimic, the loss of function cbf2 allele found in the Italian ecotype. Proposed experiments will quantify growth rates, flowering phenology, lifetime fitness, genome-wide gene expression, and untargeted metabolomics in conditions simulating the natural environments. These conditions are based on site-level climate data and recapitulate differences in relative fitness of the ecotypes at the native sites. This is an unparalleled integration of detailed studies of the genetic, molecular, and physiological mechanisms of an adaptive phenotype in a system with extensive information about local adaptation in the native environments. Training will be provided for undergraduates and postgraduates who will also participate in education outreach activities with middle and high school students.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.