My research focuses on integrating plant physiology and comparative genomics in a phylogenetic framework to understand how traits - particularly those involved in abiotic stress - evolve in plants. Much of my current work is on understanding the evolution of Crassulacean acid metabolism, a modification to the C3 photosynthetic pathway that enables plants to live in habitats where water is limiting. CAM plants open their stomata for gas exchange at night and store incoming CO2 as malate in their vacuoles; during the day, stomata (mostly) close and malate is decarboxylated, flooding the C3 pathway with high concentrations of CO2. CAM plants lose less water to the atmosphere and waste less energy on costly reactions like photorespiration.
Evolution of CAM - enablers and roadblocks
While evolving CAM photosynthesis may seem complicated – after all, it involves re-tuning the core plant metabolism, alongside a number of secondary processes, including carbon metabolism  and leaf anatomy  – CAM has evolved frequently across flowering plants (Fig. 1), suggesting it is an accessible trajectory, at least for some lineages. Recent work suggests some traits may appear in the C3 ancestor of CAM species, and may enable the evolution of CAM by already providing some of the building blocks. For example, CAM plants are often associated with having large cells, which are thought to be required to store malate; in the Agavoideae (Asparagaceae), large cells and leaf succulence are traits shared by both C3 and CAM plants, perhaps arising as a way to store water before being co-opted into the CAM pathway .
Current work on this topic includes exploring genomic enabling: are there changes at the gene level that, once present, facilitate the evolution of CAM in a lineage? I am also interested in continuing to understand the role that leaf anatomy plays in CAM evolution, how reversible CAM is, and whether CAM evolves through a similar trajectory in independent lineages.
Figure 1 - Phylogenetic origins of C4 (blue) and CAM (yellow) photosynthesis. Image credit: Ian Gilman.
Regulation of CAM gene expression
Due to the temporal shift in metabolic processes in CAM plants (i.e., CO2 uptake at night), many genes have altered expression patterns across a day compared to C3 relatives (Fig. 2). Since all C3 angiosperms have the complete set of CAM genes as part of the citric acid cycle, it’s thought that the evolution of CAM requires re-wiring of gene expression for proper CAM function [4,5]. How these genes get re-wired – and how that expression is maintained – remain a mystery.
Using the genus Yucca, in which C3, CAM, and C3+CAM intermediate species exist , we can begin to tease apart differences in gene sequences, gene regulation through chromatin modifications, metabolite fluxes, and via abiotic stress. With a JGI CSP award, we’ve sequenced the genomes of a C3 and CAM Yucca species, and are leveraging this new resource to better understand how the genomic landscape promotes and maintains CAM.
Figure 2 - Left, diagram of the CAM biochemical pathway. Incoming CO2 at night is changed to bicarbonate, then fixed via PEPC to oaxaloacetate (OAA). OAA is further converted to malate and stored in the vacuole. During the day, malate is moved from the vacuole and decarboxylated in the cytosol and subsequently moved into the chloroplast for fixation by Rubisco. Image from Heyduk et al., 2019 NRG. Right, expression of PEPC (see left panel) in two species of Yucca that differ in their photosynthetic pathway; the left species (filled circles) uses CAM, while the right species (open circles) is C3. Expression of PEPC in CAM is significantly higher than in C3. Image modified from Heyduk et al., 2019 JXB.
Ecophysiology and evolution of Joshua trees
I am a collaborator with the Joshua tree genome project and a Co-PI on a recently funded NSF award to understand the roles of biotic and abiotic selection in the evolution of Joshua trees (Yucca brevifolia and Y. jaegeriana). We're linking population genetics, demography, genomics, and ecophysiology to understand how populations of Joshua trees are adapting (or not) to local environments, with a particular eye toward understand heat and drought stress in this species. Follow along at the Joshua tree genome project website or on Twitter.
Left, Y. gloriosa in a sand dune on the coast of North Carolina. Middle, ʻōhiʻa lehua (Metrosideros polymorpha) tree growing in the center of the Kīlauea Iki volcanic lava crater, Big Island, Hawai'i. Right Joshua tree in Joshua Tree National Park. Photo credits: K. Heyduk.
1 - Heyduk K, et al. 2019 Shared expression of Crassulacean acid metabolism (CAM) genes predates the origin of CAM in the genus Yucca. Journal Exp. Botany.
2 - Heyduk K, et al. 2016 Gas exchange and leaf anatomy of a C3-CAM hybrid, Yucca gloriosa (Asparagaceae). J Exp Bot 67(5):1369–1379.
3 - Heyduk K, et al. 2016 Evolution of CAM anatomy predates the origins of Crassulacean acid metabolism in the Agavoideae (Asparagaceae). Mol Phylogenet Evol 105:102–113.
4 - Heyduk K, et al. 2019. Altered gene regulatory networks are associated with the transition from C3 to crassulacean acid metabolism in Erycina (Oncidiinae: Orchidaceae). Frontiers Plant Sci (9).
5 - Heyduk K, et al. 2018 Shifts in gene expression profiles are associated with weak and strong Crassulacean acid metabolism. American Journal Botany 105(3): 587-601.