Date of Award
Fall 2023
Document Type
Dissertation
Degree Name
Doctor of Philosophy (PhD)
Department
Ecology and Evolutionary Biology
First Advisor
Edwards, Erika
Abstract
Crassulacean acid metabolism (CAM) is an adaption to water- and CO2-limitation that has evolved independently in dozens of vascular plant lineages. The study of CAM began with 18th and 19th botanists, who noted curious changes in plant sap acidity and dark-period gas exchange in succulent plants, and continues into the genomics age with goals of engineering CAM into crops in light of global climate change. The major enzymes, metabolites, and day-night rhythms of CAM have long been established, but many fundamental questions remain, and modern molecular and computational tools allow us to ask new questions about the evolution and genetic regulation of CAM, some of which I address in this dissertation. In Chapter 1, I establish bounds on the number and phylogenetic locations of evolutionary origins of CAM across vascular plants. In a review of photosynthetic research and recent molecular phylogenies, I find evidence for at least 68 independent CAM origins in 38 families; suggesting that roughly 7% of vascular plant species are capable of CAM. Using these data, I address two long-standing hypotheses of CAM evolution: first, that CAM, like C4 photosynthesis, is an evolutionary response to the decline in atmospheric CO2 during the Eocene and Oligocene; second, that CAM evolution requires anatomical evolution. In Chapter 2, I explicitly incorporate historical atmospheric CO2 in models CAM evolution in the Caryophyllales. My results support the hypothesis that rates of CAM evolution have increased since the Oligocene, but demonstrate that more realistic models of CAM phenotypic space are needed. In Chapter 3, I analyze photosynthetic anatomy across vascular plants broadly, and in the Portullugo Clade (the clade inclusive of Portulacaceae and Molluginaceae) in detail. I provide evidence that the evolution of CAM requires anatomical evolution: generally, species capable of CAM possess larger mesophyll cells to increase malate storage capacity, and species that use CAM as their primary carbon fixation pathway further have lower intercellular airspace in order to reduce CO2 efflux. The distinctiveness of species not capable of CAM, that use CAM for a minority of carbon fixation, and that use CAM for the majority of carbon fixation allow me to predict photosynthetic physiology from anatomical data with moderate to high accuracy using machine learning. CAM anatomical evolution has been hypothesized, along with antagonistic gene regulation and metabolite fluxes, to preclude the combination of CAM and C4 photosynthesis. However, multiple lineages of C4 species capable of CAM (C4+CAM) have been discovered. In Chapter 4, I present the first whole genome sequence of a C4+CAM plant, Portulaca amilis Speg. (Portulacaceae), and describe photosynthetic gene networks in P. amilis and P. oleracea, which represent independent evolutions of C4+CAM from a CAM ancestor. I show that C4 and CAM use alternative paralogs within gene families, which suggests that multiple gene- or whole genome-duplication events are necessary to reduce pleiotropic constraints on C4+CAM evolution. I identify cis-regulatory elements in genes with roles in CAM that suggest that CAM evolves by bringing duplicated genes under derived circadian control. Finally, I use the reconstructed gene networks to hypothesize models of C4+CAM in each species. This dissertation addresses multiple fundamental questions in CAM evolution by integrating diverse molecular and computation methods and provides new resources for basic and applied photosynthetic research, including the prediction of plant physiology from anatomy and genetic engineering of CAM into C4 crops.
Recommended Citation
Gilman, Ian Spencer, "On the Evolution of Crassulacean Acid Metabolism: Diversity, Anatomy, and Genetic Components" (2023). Yale Graduate School of Arts and Sciences Dissertations. 1189.
https://elischolar.library.yale.edu/gsas_dissertations/1189
