C4-like Sesuvium sesuvioides (Aizoaceae) exhibits CAM in cotyledons and putative C4+CAM metabolism in adult leaves as revealed by transcriptome analysis

Abstract

The co-occurrence of C4 and CAM photosynthesis in a single species seems to be unusual and rare, probably because of the difficulty to co-regulate both pathways effectively. Nevertheless, it represents a unique chance in gaining new insights into the evolution and regulation of these complex pathways. Comparative transcriptomics using RNA-seq revealed C4-like and CAM photosynthesis in Sesuvium sesuvioides (Aizoaceae) leaves and cotyledons, respectively. When compared to cotyledons, phosphoenolpyruvate carboxylase 4 (PEPC4) and some key C4 genes were found to be up regulated in leaves. During the day, the expression of NADP-dependent malic enzyme (NADP-ME) was significantly higher in cotyledons than in leaves. The acidity titration confirmed higher acidity in the morning than in the previous evening indicating the induction of weak CAM in cotyledons by environmental conditions. Comparison of the leaves of S. sesuvioides (C4-like) and S. portulacastrum (C3) revealed that PEPC1 was significantly higher in S. sesuvioides, while PEPC3 and PEPC4 were up-regulated in S. portulacastrum. Finally, potential key regulatory elements involved in the C4 and CAM pathways were identified. These findings provide a new species in which C4 and CAM co-occur and raises the question if this phenomenon is indeed so rare or just hard to detect and probably more common in succulent C4 lineages. HighlightC4 and CAM metabolism co-occur in the C4-like species Sesuvium sesuvioides (Aizoaceae).