The pineapple genome and the evolution of CAM photosynthesis

TLDR

Researchers have sequenced the genomes of two cultivated pineapple varieties and a wild relative, underscoring pineapple as the most economically valuable crop with crassulacean acid metabolism, a highly water‑efficient photosynthetic pathway and the second most important tropical fruit. The study sequenced the genomes of pineapple varieties F153 and MD2 and the wild relative Ananas bracteatus accession CB5. The pineapple genome, with a conserved seven‑chromosome karyotype and one fewer ancient whole‑genome duplication than grasses, shows that the species transitioned from C3 to CAM through regulatory neofunctionalization of preexisting genes, with CAM‑related genes exhibiting diel expression and enriched cis‑regulatory elements linking CAM to circadian clock regulation.

Abstract

Ray Ming, Robert Paull, Qingyi Yu and colleagues report the genome sequences of two cultivated pineapple varieties and one wild pineapple relative. Their analysis supports the use of the pineapple as a reference genome for monocot comparative genomics and provides insight into the evolution of crassulacean acid metabolism photosynthesis. Pineapple (Ananas comosus (L.) Merr.) is the most economically valuable crop possessing crassulacean acid metabolism (CAM), a photosynthetic carbon assimilation pathway with high water-use efficiency, and the second most important tropical fruit. We sequenced the genomes of pineapple varieties F153 and MD2 and a wild pineapple relative, Ananas bracteatus accession CB5. The pineapple genome has one fewer ancient whole-genome duplication event than sequenced grass genomes and a conserved karyotype with seven chromosomes from before the ρ duplication event. The pineapple lineage has transitioned from C3 photosynthesis to CAM, with CAM-related genes exhibiting a diel expression pattern in photosynthetic tissues. CAM pathway genes were enriched with cis-regulatory elements associated with the regulation of circadian clock genes, providing the first cis-regulatory link between CAM and circadian clock regulation. Pineapple CAM photosynthesis evolved by the reconfiguration of pathways in C3 plants, through the regulatory neofunctionalization of preexisting genes and not through the acquisition of neofunctionalized genes via whole-genome or tandem gene duplication.