Multiomics unravels potential molecular switches in the C to CAM transition of Mesembryanthemum crystallinum.

Mesembryanthemum crystallinum (common ice plant), a facultative CAM plant, shifts from C to CAM photosynthesis under salt stress, enhancing water use efficiency. Here we used transcriptomics, proteomics, and targeted metabolomics to profile molecular changes during the diel cycle of C to CAM transition. The results confirmed expected changes associated with CAM photosynthesis, starch biosynthesis and degradation, and glycolysis/gluconeogenesis. Importantly, they yielded new discoveries: 1) Transcripts displayed greater circadian regulation than proteins. 2) Oxidative phosphorylation and inositol methylation may play important roles in initiating the transition. 3) V-type H-ATPases showed consistent transcriptional regulation, aiding in vacuolar malate uptake. 4) A protein phosphatase 2C, a major component in the ABA signaling pathway, may trigger the C to CAM transition. Our work highlights the potential molecular switches in the C to CAM transition, including the potential role of ABA signaling. SIGNIFICANCE: The common ice plant is a model facultative CAM plant, and under stress conditions it can shift from C to CAM photosynthesis within a three-day period. However, knowledge about the molecular changes during the transition and the molecular switches enabling the transition is lacking. Multi-omic analyses not only revealed the molecular changes during the transition, but also highlighted the importance of ABA signaling, inositol methylation, V-type H-ATPase in initiating the shift. The findings may explain physiological changes and nocturnal stomatal opening, and inform future synthetic biology effort in improving crop water use efficiency and stress resilience.