Gene expression in response to drought stress among seedlings derived from different source populations of a California endemic oak, Quercus lobata

Background/Question/Methods

Climate change is a particularly challenging threat to tree species because their long generation time can delay their evolutionary response.  Tolerating the projected rapid rate of 21^st Century climate warming and drying will require that tree populations utilize existing local adaptation to climate for the survival of tree populations. Quercus lobata (valley oak) offers a unique opportunity to study local adaptation of response to climate because it occupies a heterogeneous range of environmental conditions and exhibits localized differentiation among populations. To test for different morphological adaptations to local climate and differential responses to climate change among populations, we grew seedlings that were derived from four populations from different climate environments in a common greenhouse.  We then quantified differences in leaf morphological traits, and measured gene expression changes in leaves using whole-transcriptome sequencing (RNA-Seq) before and after 10 days of water deprivation. We then tested whether differentially expressed genes were associated with leaf morphological variation related to drought tolerance.

Results/Conclusions

Phenotypic traits such as acorn weight, days to germination, leaf dry mass, leaf area, leaf thickness, and all the climatic variables differed significantly among populations of Q. lobata. Redundancy analysis showed associations between morphological traits and important climatic variables, such as growing season precipitation, mean maximum temperature in the warmest month and degrees C accumulating within the frost-free period. These differences reflect genetically based morpho-functional adaptations to climatic conditions of the locality. Changes in gene expression profiles for 11 seedlings from the 4 populations before and after water stress suggest different responses to water stress in dry, southern Malibu Creek State Park and Springville, versus wet, northern Middle Creek and Hastings Reserve populations. For each population, we identified significant down-regulated and up-regulated genes after water stress: respectively, 5518 and 5018 in Springville; 127 and 853 in Malibu Creek; 3772 and 2371 in Middle Creek; and 12,332 and 7342 in Hastings. Annotation from all up-regulated genes revealed that northern populations showed fewer gene categories related to drought stress than southern populations (e.g., genes that respond to abiotic stimulus, stress, light, radiation, water deprivation, and UV). These results suggest that there are different molecular strategies to cope with water deficit during the dry season in different populations.  We conclude that different regional populations have different gene expression responses and different genotypes underlying traits associated with response to drought that may affect their ability to respond to rapid climate change.