Gene duplications facilitate C(4)-CAM compatibility in common purslane

Common purslane (Portulaca oleracea) integrates both C(4) and crassulacean acid metabolism (CAM) photosynthesis pathways and is a promising model plant to explore C(4)-CAM plasticity. Here, we report a high-quality chromosome-level genome of nicotinamide adenine dinucleotide (NAD)-malic enzyme (ME) subtype common purslane that provides evidence for 2 rounds of whole-genome duplication (WGD) with an ancient WGD (P-β) in the common ancestor to Portulacaceae and Cactaceae around 66.30 million years ago (Mya) and another (Po-α) specific to common purslane lineage around 7.74 Mya. A larger number of gene copies encoding key enzymes/transporters involved in C(4) and CAM pathways were detected in common purslane than in related species. Phylogeny, conserved functional site, and collinearity analyses revealed that the Po-α WGD produced the phosphoenolpyruvate carboxylase-encoded gene copies used for photosynthesis in common purslane, while the P-β WGD event produced 2 ancestral genes of functionally differentiated (C(4)- and CAM-specific) beta carbonic anhydrases involved in the C(4) + CAM pathways. Additionally, cis-element enrichment analysis in the promoters showed that CAM-specific genes have recruited both evening and midnight circadian elements as well as the Abscisic acid (ABA)-independent regulatory module mediated by ethylene-response factor cis-elements. Overall, this study provides insights into the origin and evolutionary process of C(4) and CAM pathways in common purslane, as well as potential targets for engineering crops by integrating C(4) or CAM metabolism.