Format: ORAL

Clara Groot Crego1,2, Jaqueline Hess1,3, Gil Yardeni1,4, Marylaure de La Harpe1,5, Clara Priemer6,7, Francesca Beclin1,2,8, Sarah Saadain1,2, Luiz A. Cauz-Santos1, Eva M. Temsch1, Hanna Weiss-Schneeweiss1, Michael H.J. Barfuss1, Walter Till1, Wolfram Weckwerth6,7, Karolina Heyduk9, Christian Lexer1,, Ovidiu Paun1, Thibault Leroy1,10

1 Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria 2 Vienna Graduate School of Population Genetics, Vienna, Austria 3 Cambrium GmbH, Max-Urich-Str. 3, 13055 Berlin, Germany 4 Institute of Computational Biology, Department of Biotechnology, University of Life Sciences and Natural Resources (BOKU), Muthgasse 18, 1190 Vienna, Austria. 5 Office for Nature and Environment, Canton of Grisons, Chur, Switzerland 6 Department of Functional and Evolutionary Ecology, Molecular Systems Biology (MOSYS), University of Vienna, Vienna, Austria 7 Vienna Metabolomics Center (VIME), University of Vienna, Vienna, Austria 8 Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Vienna, Austria 9 Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT USA 10 GenPhySE, Université de Toulouse, INRAE, ENVT, Castanet Tolosan, France †deceased

The subgenus Tillandsia (Bromeliaceae) belongs to one of the fastest radiating clades in the plant kingdom and is characterised by the repeated evolution of the water-conserving Crassulacean Acid Metabolism (CAM), which is regarded as a key innovation trait and driver of ecological diversification in Bromeliaceae. By obtaining physiological and transcriptomic data under control and drought conditions of a Tillandsia species pair representing the phenotypic extremes of photosynthetic metabolism found in the clade, we were able to characterise the range of CAM phenotypes in Tillandsia with unprecedented detail. We found that species previously identified as C3 are CAM intermediates which activate a latent CAM cycle under drought conditions. However, the CAM-specific response to drought in this facultative species has little overlap with the constitutive CAM cycle of the strong CAM species. By producing high quality genome assemblies of a facultative and a constitutive CAM Tillandsia, and combining genome-wide investigations of synteny, TE dynamics, sequence evolution, gene family evolution and temporal differential expression, we were able to pinpoint the genomic drivers of CAM evolution in Tillandsia. Our analyses show that rewiring of photosynthetic metabolism towards constitutive CAM is mainly obtained through regulatory evolution rather than coding sequence evolution, as CAM-related genes are differentially expressed across a 24-hour cycle between the two species, but are no candidates of positive selection. Gene orthology analyses reveal that CAM-related gene families manifesting differential expression underwent accelerated gene family expansion in the constitutive CAM species, further supporting the view of gene family evolution as a driver of CAM evolution.