2026 Theses Doctoral

The Genetics of Recognition: Parasitism, Reproduction, and Genome Evolution in Flowering Plants

Cohen, Rachel O.

Plant–plant interactions are typically viewed through the lens of competition for resources such as space, light, and nutrients, yet plants also engage in interactions that require molecular-level recognition of foreign tissues, including parasitism and interspecific reproductive interactions. This dissertation investigates the genetic underpinnings of these two understudied interactions and asks how they shape organismal evolution. I focus on plants in the genus Pedicularis, a hyperdiverse lineage of alpine flowering plants that frequently exchange pollen with both close and distant relatives. Pedicularis are facultative hemiparasites, and, like all parasitic angiosperms, attach to host roots via haustoria, specialized organs that penetrate host tissue to siphon water and mineral nutrients. There is some evidence that reproductive interactions and parasitism share common molecular pathways, yet this relationship has never been explored. Across four chapters, I examine how plants recognize foreign interactants during reproduction and parasitism, ask how these interactions are related at the molecular-level, and investigate how they impact genome evolution in Pedicularis.

In Chapter 1, I generate the first reference genome for Pedicularis groenlandica (Elephant’s head lousewort) and produce a time-series transcriptomic dataset spanning haustorial development and attachment. Using these data, I identify genes associated with haustoria, test the hypothesis that plants evolve parasitic function through recruitment of genes originally functioning in other tissues, and compare haustoria-associated gene expression in P. groenlandica to that of other parasitic plant lineages using a comparative transcriptomic framework. I show that approximately 20% of the P. groenlandica genome is involved in parasitic attachment and that these genes are enriched for signaling, cell wall modification, and plant defense pathways. Notably, haustoria-associated genes overlap most strongly with genes involved in pollen tube growth, providing direct evidence for a shared molecular basis of parasitism and plant reproduction. I conclude that P. groenlandica has primarily co-opted pollen tube-associated genes for parasitic function, rather than root-associated genes as previously hypothesized, and that many haustorial genes are lineage-specific, highlighting repeated and divergent molecular routes to parasitism across flowering plants.

In Chapter 2, I examine plant reproductive interactions by quantifying the fate of heterospecific pollen in natural communities. In species-rich alpine meadows, plants frequently share pollinators and exchange pollen, a process known as heterospecific pollen transfer (HPT). HPT often reduces seed set in recipient plants and can impose strong selection on reproductive traits such as floral color and morphology. However, we currently lack robust predictors of the post-pollination fate of heterospecific pollen, especially in community and phylogenetic contexts. Through experimental crosses among 11 co-flowering species in alpine meadows, I track heterospecific pollen success across three reproductive stages: stigma germination, pollen tube growth, and ovule fertilization. I find that heterospecific pollen tubes can germinate and grow through pistils even when donor and recipient species are separated by over 100 million years of evolution, and that phylogenetic distance does not predict pollen success. These results indicate that maternal mechanisms do not actively reject heterospecific pollen during early post-pollination stages.

In Chapter 3, I use comparative transcriptomics to investigate the molecular responses of maternal plants to heterospecific pollen across genetic distance. By pollinating P. groenlandica and Mimulus guttatus with pollen from close and distant relatives and quantifying differential gene expression, I show that the magnitude of the transcriptional response decays with phylogenetic distance. Genes responding to conspecific and closely-related pollen are enriched for known pollination and pollen tube growth pathways, whereas responses to distant pollen lack clear reproductive function. I propose that this pattern reflects positive recognition of compatible pollen rather than active rejection of incompatible pollen. To test this hypothesis, I conducted a pollen tube growth rate experiment, showing quantitatively that heterospecific pollen tubes grow more slowly than conspecific pollen tubes. I conclude that molecular-level recognition of pollen decays with increasing phylogenetic distance between crossing parents, impeding heterospecific pollen from reaching the ovules as quickly as conspecific pollen, thereby promoting reproductive isolation.

In Chapter 4, I investigate the role of horizontal gene transfer (HGT) in parasitic plant genome evolution. I generated chromosome-scale genomes for six additional Pedicularis species and assembled a comparative dataset of 59 plant genomes, including 15 more parasitic species within the parasitic plant family Orobanchaceae. Using a novel model-based approach, I identify candidate HGT events based on discordance between gene trees and species trees. I map HGT across the Orobanchaceae phylogeny, and show that HGTs are primarily associated with core cellular pathways, rather than pathways commonly associated with the parasitic process, like signaling or defense. This work represents the largest phylogenomic investigation of HGT in Orobanchaceae to date and provides new insight into how HGT impacts parasitic plant genome evolution.

Together, my chapters demonstrate that parasitism and reproductive interactions share deep molecular parallels, exert strong selective pressures, and play underappreciated roles in shaping genome evolution and diversification in flowering plants.