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

• DOI: 10.1111/pce.13847
• Publication Date: 2020-07-17T05:29:00Z
• Authors: Marylaure De La H...; Margot Paris; Jaqueline Hess; Michael Harald Jo...; Martha Liliana Se...; Arindam Ghatak; Palak Chaturvedi; Wolfram Weckwerth; Walter Till; Nicolas Salamin; Ching Man Wai; Ray Ming; Christian Lexer
• Keywords: EXPRESSION; Bromeliaceae; GENES; TREE ESTIMATION; Genetic Speciation; drought; Genes, Plant; circadian period length; Crassulacean Acid Metabolism; 03 medical and health sciences; BROMELIACEAE; Exome Sequencing; PHYLOGENETIC ANALYSIS; SDG 15 – Leben an Land; genome; Phylogeny; SDG 15 - Life on Land; 0303 health sciences; CAM; Whole Genome Sequencing; Sequence Analysis, RNA; copy number variation; 106008 Botanik; 15. Life on land; Biological Evolution; 106008 Botany; FAMILY; READ ALIGNMENT; CRASSULACEAN ACID METABOLISM; PHOTOSYNTHETIC PATHWAYS; adaptive radiation; transcriptome

AbstractThe 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.