CAM evolution is associated with gene family expansion in an explosive bromeliad radiation

Author(s)
Clara Groot Crego, Jaqueline Hess, Gil Yardeni, Marylaure de La Harpe, Clara Priemer, Francesca Beclin, Sarah Saadain, Luiz A Cauz-Santos, Eva M Temsch, Hanna Weiss-Schneeweiss, Michael H J Barfuss, Walter Till, Wolfram Weckwerth, Karolina Heyduk, Christian Lexer, Ovidiu Paun, Thibault Leroy
Abstract

The subgenus Tillandsia (Bromeliaceae) belongs to one of the fastest radiating clades in the plant kingdom and is characterised by the repeated evolution of Crassulacean acid metabolism (CAM). Despite its complex genetic basis, this water-conserving trait has evolved independently across many plant families and is regarded as a key innovation trait and driver of ecological diversification in Bromeliaceae. By producing high-quality genome assemblies of a Tillandsia species pair displaying divergent photosynthetic phenotypes, and combining genome-wide investigations of synteny, transposable element (TE) dynamics, sequence evolution, gene family evolution and temporal differential expression, we were able to pinpoint the genomic drivers of CAM evolution in Tillandsia. Several large-scale rearrangements associated with karyotype changes between the two genomes and a highly dynamic TE landscape shaped the genomes of Tillandsia. However, our analyses show that rewiring of photosynthetic metabolism 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 not 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.

Organisation(s)
Department of Botany and Biodiversity Research, Department of Microbiology and Ecosystem Science, Functional and Evolutionary Ecology
External organisation(s)
Office for Nature and Environment, Canton of Grisons, Chur, Switzerland., Österreichische Akademie der Wissenschaften (ÖAW), University of Connecticut, University of Toulouse, Cambrium GmbH, Universität für Bodenkultur Wien
Journal
The Plant Cell
ISSN
1040-4651
DOI
https://doi.org/10.1093/plcell/koae130
Publication date
04-2024
Peer reviewed
Yes
Austrian Fields of Science 2012
106014 Genomics, 106012 Evolutionary research, 106003 Biodiversity research
Portal url
https://ucrisportal.univie.ac.at/en/publications/cam-evolution-is-associated-with-gene-family-expansion-in-an-explosive-bromeliad-radiation(34e5130a-4da6-4326-99d9-f7dad55db31c).html