Genomic and transcriptomic analyses of Phytophthora cinnamomi reveal complex genome architecture, expansion of pathogenicity factors, and host-dependent gene expression profiles

<i>Phytophthora cinnamomi</i> is a hemibiotrophic oomycete causing Phytophthora root rot in over 5,000 plant species, threatening natural ecosystems, forestry, and agriculture. Genomic studies of <i>P. cinnamomi</i> are limited compared to other <i>Phytophthora</i> spp. despite the importance of this destructive and highly invasive pathogen. The genome of two genetically and phenotypically distinct <i>P. cinnamomi</i> isolates collected from avocado orchards in California were sequenced using PacBio and Illumina sequencing. Genome sizes were estimated by flow cytometry and assembled <i>de novo</i> to 140-141 Mb genomes with 21,111-21,402 gene models. Genome analyses revealed that both isolates exhibited complex heterozygous genomes fitting the two-speed genome model. The more virulent isolate encodes a larger secretome and more RXLR effectors when compared to the less virulent isolate. Transcriptome analysis after <i>P. cinnamomi</i> infection in <i>Arabidopsis thaliana, Nicotiana benthamiana</i>, and <i>Persea americana</i> de Mill (avocado) showed that this pathogen deploys common gene repertoires in all hosts and host-specific subsets, especially among effectors. Overall, our results suggested that clonal <i>P. cinnamomi</i> isolates employ similar strategies as other <i>Phytophthora</i> spp. to increase phenotypic diversity (e.g., polyploidization, gene duplications, and a bipartite genome architecture) to cope with environmental changes. Our study also provides insights into common and host-specific <i>P. cinnamomi</i> infection strategies and may serve as a method for narrowing and selecting key candidate effectors for functional studies to determine their contributions to plant resistance or susceptibility.