Sequencing of the Pineapple Genome as a Model CAM species

Pineapple 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 A. bracteatus accession CB5. The pineapple genome has one fewer ancient whole genome duplications than sequenced grass genomes and a conserved karyotype with seven pre rho duplication chromosomes. The pineapple lineage has transitioned from C3 photosynthesis to CAM with CAM-related genes exhibiting a diel expression pattern in photosynthetic tissues using beta-carbonic anhydrase(βCA) for initial capture of CO2. Promoter regions of all three βCA genes contain a CCA1 binding site that can bind circadian core oscillators. CAM pathway genes were enriched with cis-regulatory elements including the morning (CCACAC) and evening (AAAATATC) elements associated with regulation of circadian-clock genes, providing the first cis-regulatory link between CAM and the circadian clock regulation. Gene-interaction network analysis revealed both activation and repression of regulatory elements that control key enzymes in CAM photosynthesis. Pineapple CAM photosynthesis evolved by reconfiguration of pathways in C3 plants through regulatory neofunctionalization of preexisting genes and not acquisition of neofunctionalized genes via whole genome or tandem gene duplication.