Evolution and function of an unusual photosynthetic metabolism: Portulaca, the C4-CAM plant

Yale University, New Haven CT

Investigators

Abstract

Plants perform photosynthesis to transform carbon dioxide and sunlight into stored chemical energy - carbohydrates - that the rest of life relies upon. Photosynthesis works well when plants are not exposed to environmental stress, but when plants are too hot, or drought stressed, this process becomes inefficient. Plants have evolved two main alternative photosynthetic pathways in response to environmental stresses, CAM and C4 photosynthesis. C4 and CAM have each evolved many times, and it has been thought that C4 evolved in response to hot temperatures and CAM in response to drought. Similarly, these two pathways were assumed to be incompatible at cellular and genetic levels. However, a C4-CAM plant has been discovered: Portulaca, which performs C4 photosynthesis normally, but performs CAM under drought. This project aims to understand the function and ecological significance of a C4-CAM photosynthetic system. The research team will discover how many times C4-CAM evolved in Portulaca, and will identify the spatial configuration of both pathways within the leaf. They will identify the genes that regulate both pathways, and will compare the ecological ranges of C4-CAM species with relatives that do not have this trait. Finally, they will survey other plants to identify additional origins of this novel photosynthesis type. This research may contribute to crop improvement- for example, efforts to engineer C4 into rice, and CAM into poplar. A C4-CAM crop could be highly productive when water is prevalent, but drought-resistant when water is scarce. In addition, this award will support a broad range of educational activities, including post-doctoral and graduate student training, undergraduate research, and high school teacher training and curriculum development. C4 and CAM photosynthesis are two metabolic pathways that have evolved multiple times. Though biochemically similar, each pathway requires a unique suite of anatomical characters in order to work efficiently, and conventional wisdom holds that these characters are antagonistic, such that anatomy that facilitates efficient C4 will simultaneously disadvantage a CAM metabolism. This widely accepted view cannot, however, accommodate Portulaca, the only plants currently known to operate both C4 and CAM cycles within a single leaf. Recent work suggests that ancestral Portulaca was a facultative CAM plant, and evolved a C4 system while maintaining CAM capability at least three times. The proposed research will test this hypothesis and develop Portulaca as a model lineage for investigating the evolutionary connectivity of C4 and CAM pathways. This project aims to: 1) confirm the existence of facultative CAM in all major Portulaca lineages, and characterize CAM and C4 biochemical cycles and differential gene expression in 7 species representing all C4 origins; 2) identify the spatial configuration of C4 and CAM cycles within the leaf, using in situ hybridization and protein immunolocalization; 3) utilize recently designed targeted gene enrichment baits (HybSeq) to sequence key photosynthetic (and other) genes from across Portulaca to improve phylogenetic resolution and analyze convergent molecular adaptation across the group; 4) characterize and contrast the climatic envelopes occupied by C4-CAM Portulaca and C3-CAM related lineages; and 5) initiate phylogenetically-informed physiological surveys to discover additional C4-CAM plants in other clades. This award was co-funded in the Biology Directorate of NSF by Integrative Ecological Physiology in the Integrative Organismal Systems Division, Systematics and Biodiversity Science in the Division of Environmental Biology, and Emerging Frontiers. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.