Inferring the genetic responses to acute drought stress across an ecological gradient

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Background: How do xerophytic species thrive in environments that experience extreme annual drought? Although critical to the survival of many species, the genetic responses to drought stress in many non-model organisms has yet to be explored. We investigated this question in Mentzelia section Bartonia (Loasaceae), which occurs throughout western North America, including arid lands. To better understand the genetic responses to drought stress among species that occur in different habitats, the gene expression levels of three species from Mentzelia were compared across a precipitation gradient. Two de novo reference transcriptomes were generated and annotated. Leaf and root tissues were collected from control and drought shocked plants and compared to one another for differential expression. A target-gene approach was also implemented to better understand how drought-related genes from model and crop species function in non-model systems. Results: When comparing the drought-shock treatment plants to their respective control plants, we identified 165 differentially expressed clusters across all three species. Differentially expressed genes including those associated with water movement, photosynthesis, and delayed senescence. The transcriptome profiling approach was coupled with a target genes approach that measured expression of 90 genes associated with drought tolerance in model organisms. Comparing differentially expressed genes with a ≥ 2 log-fold value between species and tissue types showed significant differences in drought response. In pairwise comparisons, species that occurred in drier environments differentially expressed greater genes in leaves when drought shocked than those from wetter environments, but expression in the roots mostly produced opposite results. Conclusions: Arid-adapted species mount greater genetic responses compared to the mesophytic species, which has likely evolved in response to consistent annual drought exposure across generations. Drought responses also depended on organ type. Xerophytes, for example, mounted a larger response in leaves to downregulate photosynthesis and senescence, while mobilizing carbon and regulating water in the roots. The complexity of drought responses in Mentzelia suggest that whole organism responses need to be considered when studying drought and, in particular, the physiological mechanisms in which plants regulate water, carbon, cell death, metabolism, and secondary metabolites.