Closely related facultative and constitutive CAM phenotypes show little transcriptomic overlap in the subgenusTillandsia

Abstract The evolutionary trajectory and genetic architecture of crassulacean acid metabolism (CAM), a water-efficient form of photosynthesis that has evolved repeatedly in the plant kingdom, remains elusive. The extent to which different CAM phenotypes share a genetic basis, forming a continuum through varying degrees of expression, or exhibit divergence and redundancy of employed genes and their expression, is still debated. The subgenus Tillandsia provides an excellent opportunity to compare the genetic basis of different CAM forms, given its broad range of photosynthetic phenotypes. Through physiological and transcriptomic analyses of well-watered and water-limited accessions of a closely related species pair, we comprehensively characterized facultative and constitutive CAM in Tillandsia . By comparing orthologous gene expression and orthogroup recruitment, we found that while both species performed CAM upon water-withholding, transcriptional modulation of orthogroups related to stomatal movement, sugar/malate transport, aquaporins and starch metabolism showed little similarity. Enzymes of the CAM (de)carboxylation modules exhibited shared expression patterns, though distinct orthologs of PEPC were upregulated at night in each species. Our study reveals that, while the expression of certain core CAM enzymes is shared, these species exhibit substantial divergence of CAM-related transcriptomic modulation, revealing CAM’s polygenic nature and providing a possible hypothesis for its evolvability. 1. Highlight We comprehensively characterized and compared facultative and constitutive CAM phenotypes in Tillandsia bromeliads on a physiological and transcriptomic level. We found substantial divergence in CAM-related transcriptomic modulation between phenotypes, highlighting the polygenic nature of the CAM continuum.