Closely related facultative and constitutive CAM phenotypes show little transcriptomic overlap in the subgenusTillandsia

Abstract

The evolutionary trajectory of Crassulacean acid metabolism (CAM) remains elusive, as it has evolved repeatedly, yet represents a complex trait requiring changes on several organismal levels. It is debated whether distinct forms of CAM embody a single quantitative trait, or entirely separate, categorical phenotypes. The subgenus Tillandsia provides an excellent opportunity to compare the genetic basis of different forms of CAM, as species are closely related, yet display a broad range of CAM phenotypes. By combining physiological and transcriptomic analyses of well-watered and drought-stressed accessions of a Tillandsia species pair, we achieved a comprehensive characterization of their photosynthetic phenotypes and the transcriptomic underpinnings and overlap of distinct CAM phenotypes in Tillandsia. We found that a species previously identified as C3 displays an active CAM cycle under drought stress, yet the effect of drought was markedly increased compared to the constitutive CAM species . The CAM-specific transcriptomic response to day-night changes and to drought showed little overlap between the two species, with most DE genes showing distinct regulation patterns or being unique to one species. Our study reveals that the two species do not exhibit a shared transcriptomic basis of CAM expressed at distinct levels, but that different transcriptomic routes can lead to similar phenotypes, supporting the view that CAM is a highly polygenic trait.