Origin and mechanism of crassulacean acid metabolism in orchids as implied by comparative transcriptomics and genomics of the carbon fixation pathway.

Crassulacean acid metabolism (CAM) is a CO2 fixation pathway that maximizes water-use efficiency (WUE), compared with the C3/C4 CO2 pathway, which permits CAM plants to adapt to arid environments. The CAM pathway provides excellent opportunities to genetically design plants, especially bioenergy crops, with a high WUE and better photosynthetic performance than C3/C4 in arid environments. The information available on the origin and evolution of CAM is scant, however. Here, we analyzed transcriptomes from 13 orchid species and two existing orchid genomes, covering CAM and C3 plants, with an emphasis on comparing 13 gene families involved in the complete carbon fixation pathway. The dosage of the core photosynthesis-related genes plays no substantial role in the evolution of CAM in orchids; however, CAM may have evolved primarily by changes at the transcription level of key carbon fixation pathway genes. We proposed that in both dark and light, CO2 is primarily fixed and then released through two metabolic pathways via known genes, such as PPC1, PPDK and PPCK. This study reports a comprehensive comparison of carbon fixation pathway genes across different photosynthetic plants, and reveals the importance of the level of expression of key genes in the origin and evolution of CAM.