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

Harpe, Marylaure de La; Paris, Margot; Hess, Jaqueline; Barfuss, Michael Harald Johannes; Serrano‐Serrano, Martha Liliana; Ghatak, Arindam; Chaturvedi, Palak; Weckwerth, Wolfram; Till, Walter; Salamin, Nicolas; Wai, Ching Man; Ming, Ray; Lexer, Christian

doi:10.1111/pce.13847

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

Harpe, Marylaure de La Department of Botany and Biodiversity Research, Division of Systematic and Evolutionary Botany, Faculty of Life Sciences, University of Vienna Vienna Austria - Department of Biology, Unit of Ecology & Evolution, University of Fribourg Fribourg Switzerland
Paris, Margot Department of Botany and Biodiversity Research, Division of Systematic and Evolutionary Botany, Faculty of Life Sciences, University of Vienna Vienna Austria - Department of Biology, Unit of Ecology & Evolution, University of Fribourg Fribourg Switzerland
Hess, Jaqueline Department of Botany and Biodiversity Research, Division of Systematic and Evolutionary Botany, Faculty of Life Sciences, University of Vienna Vienna Austria
Barfuss, Michael Harald Johannes Department of Botany and Biodiversity Research, Division of Systematic and Evolutionary Botany, Faculty of Life Sciences, University of Vienna Vienna Austria
Serrano‐Serrano, Martha Liliana Department of Computational Biology, Faculty of Biology and Medicine, University of Lausanne Lausanne Switzerland
Ghatak, Arindam Department of Functional and Evolutionary Ecology, Division of Molecular Systems Biology (MOSYS), Faculty of Life Sciences, University of Vienna Vienna Austria - Vienna Metabolomics Center (VIME)University of Vienna Vienna Austria
Chaturvedi, Palak Department of Functional and Evolutionary Ecology, Division of Molecular Systems Biology (MOSYS), Faculty of Life Sciences, University of Vienna Vienna Austria - Vienna Metabolomics Center (VIME)University of Vienna Vienna Austria
Weckwerth, Wolfram Department of Functional and Evolutionary Ecology, Division of Molecular Systems Biology (MOSYS), Faculty of Life Sciences, University of Vienna Vienna Austria - Vienna Metabolomics Center (VIME)University of Vienna Vienna Austria
Till, Walter Department of Botany and Biodiversity Research, Division of Systematic and Evolutionary Botany, Faculty of Life Sciences, University of Vienna Vienna Austria
Salamin, Nicolas Department of Computational Biology, Faculty of Biology and Medicine, University of Lausanne Lausanne Switzerland
Wai, Ching Man Department of Horticulture, College of Agriculture and Natural Resources, Michigan State University East Lansing Michigan USA
Ming, Ray Department of Plant Biology, School of Integrative Biology, University of Illinois at Urbana‐Champaign Urbana Illinois USA
Lexer, Christian Department of Botany and Biodiversity Research, Division of Systematic and Evolutionary Botany, Faculty of Life Sciences, University of Vienna Vienna Austria - Department of Biology, Unit of Ecology & Evolution, University of Fribourg Fribourg Switzerland

2020

Published in:

Plant, Cell & Environment. - 2020, vol. 43, no. 12, p. 2987-3001

English 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.

Faculty

Faculté des sciences et de médecine

Department

Département de Biologie

Language