Genomic footprints of repeated evolution of CAM photosynthesis in a Neotropical species radiation

The adaptive radiation of Bromeliaceae (pineapple family) is one of the most diverse among Neotropical flowering plants. Diversification in this group was facilitated by shifts in several adaptive traits or "key innovations" including the transition from C₃ to CAM photosynthesis associated with xeric (heat/drought) adaptation. We used phylogenomic approaches complemented by differential gene expression (RNA-seq) and targeted metabolite profiling to address the mechanisms of C₃ /CAM evolution in the extremely species-rich bromeliad genus Tillandsia and related taxa. Evolutionary analyses of whole-genome sequencing and RNA-seq data suggest that evolution of CAM is associated with coincident changes to different pathways mediating xeric adaptation in this group. At the molecular level, C₃ /CAM shifts were accompanied by gene expansion of XAP5 CIRCADIAN TIMEKEEPER homologs, a regulator involved in sugar- and light-dependent regulation of growth and development. Our analyses also support the re-programming of abscisic acid-related gene expression via differential expression of ABF2/ABF3 transcription factor homologs, and adaptive sequence evolution of an ENO2/LOS2 enolase homolog, effectively tying carbohydrate flux to abscisic acid-mediated abiotic stress response. By pinpointing different regulators of overlapping molecular responses, our results suggest plausible mechanistic explanations for the repeated evolution of correlated adaptive traits seen in a textbook example of an adaptive radiation. This article is protected by copyright. All rights reserved.

Keywords: Bromeliaceae; adaptive radiation; circadian period length; copy number variation; drought; genome; transcriptome.