Phytophthora cinnamomi, the causal agent of Phytophthora root rot, is a cosmopolitan plant pathogen with a wide host range that threatens native ecosystems and major agricultural crops including avocado. Despite the importance of this invasive alien pathogen, the number of genomic resources for P. cinnamomi are minimal and mechanisms for generating novel genetic diversity remain unclear. Many P. cinnamomi populations have been described as clonal, however despite the lack of sexual reproduction, P. cinnamomi is notorious for its ability to adapt to novel environments and stressors while exhibiting genotypic and phenotypic variability. We generated novel genomic resources for two representative P. cinnamomi isolates to elucidate mechanisms for generating novel genetic diversity and uncover host infection strategies. With these genomic resources we uncovered the genetic and phenotypic variability of P. cinnamomi populations affecting avocado in California and Mexico. The results of this dissertation are presented in two chapters: 1) genomic analyses of two genotypically and phenotypically distinct isolates of P. cinnamomi and transcriptomic analyses of P. cinnamomi infecting various host plants over time; 2) characterizing the phenotypic and genotypic variability of P. cinnamomi populations affecting avocado in California and Mexico. Novel de novo genome assemblies supported by flow cytometry genome size estimations were generated for two representative P. cinnamomi isolates from California avocado. Genomic analyses revealed expanded genome size with complex profile, a bipartite “two-speed” architecture, high synteny between the two isolates, orthologous proteins, and variation in secretome and effector repertoire sizes. Transcriptomic analysis of P. cinnamomi infecting Nicotiana benthamiana, Persea americana and Arabidopsis thaliana revealed host-specific and common in planta gene expression patterns. Population structure analyses revealed that the P. cinnamomi isolates from California and Mexico are clonal and Mexico was likely the source of an introduction event into Southern California avocado growing regions. The P. cinnamomi population from California were less diverse than the population from Mexico and these populations likely belong to the two panglobal lineages of A2 P. cinnamomi. Phenotypic characterization of select isolates revealed variability in fungicide sensitivity, in vitro growth rate, sensitivity to higher growth temperature and virulence in avocado seedlings and pears, despite clonality.

Challenges by pathogens and pests have presented major problems for crop production, posing major constraints to meeting the food requirements for the increasing global population. The most devastating pathogens for agriculture belong to the Phytophthora genus (The so-called “plant destroyers”). The goal of this dissertation research is to advance our understanding in ways to enhance resistance against two extremely effective Phytophthora species, P. infestans and P. cinnamomi. Disease control/management strategies against these two oomycete pathogens remain unsustainable and argue for new control methods including the generation of crops with durable and effective resistance against them. This dissertation focuses on two main objectives 1. Identifying and characterizing specific plant defense proteins equipped to combat against P. infestans, 2. To study the in-planta expression of the Pc effector repertoire during its interaction with different host plants to identify effectors that contribute to P. cinnamomi virulence, and that can be eventually used to fetch key resistance and susceptibility plant targets to engineer P. cinnamomi resistant plants in the future.In Chapter 2, we investigated the interacting proteins of microchidia 1 (MORC1) proteins from Arabidopsis thaliana, Solanum tuberosum (potato), and Solanum lycopersicum (tomato). We identified and characterized a MORC1 interacting protein, better known as in Arabidopsis as Drink Me-Like (DKML) basic leucine zipper (bZIP) transcription factor 29. Interestingly, DKML homologs in tomato, potato, and Nicotiana benthamiana interacted with the C-terminal region of MORC1 in tomato and potato. Additionally, we investigated DKMLs roles in plant immunity by way of virus induced gene silencing (VIGS) and transient expression and discovered that it regulates plant cell death and resistance for P. infestans. In Chapter 3, we The best way to combat these devastating pathogens is to understand the mechanisms that allow them to be so effective. Disease-causing pathogens, including oomycetes, rely upon “effector proteins” that contribute to their virulence by manipulating nutrient delivery or suppressing the host plant’s immune response. One possible route for protecting crops involves genetically modifying the targets of these effector proteins so they can still perform their function for the plant, but cannot be manipulated by pathogen effectors. These effector plant targets are called susceptibility (S) genes. Another route for protecting crops involves boosting the plants’ natural defense by expressing plant proteins that recognize and fight against these pathogen effectors (Resistance (R) genes). Identification of these key R and S targets are critical to understanding the function of these genes during plant immunity, getting us one step closer to generating the most durable resistant crops.