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

Clara Groot Crego (Corresponding author), 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

Publications: Contribution to journalArticlePeer Reviewed

Abstract

The subgenus Tillandsia (Bromeliaceae) belongs to one of the fastest radiating clades in the plant kingdom and is characterized 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 2 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-h cycle between the 2 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.

Original languageEnglish
Pages (from-to)4109-4131
Number of pages23
JournalThe Plant Cell
Volume36
Issue number10
Early online date30 Apr 2024
DOIs
Publication statusPublished - 3 Oct 2024

Austrian Fields of Science 2012

  • 106012 Evolutionary research
  • 106014 Genomics
  • 106003 Biodiversity research

Fingerprint

Dive into the research topics of 'CAM evolution is associated with gene family expansion in an explosive bromeliad radiation'. Together they form a unique fingerprint.

Cite this