Phylogenomic analysis of Phytophthora cinnamomi collected from avocado in the United States reveals links to the two A2 panglobal clonal lineages

Abstract

Phytophthora cinnamomi, the causal agent of phytophthora root rot (PRR), is one of the most destructive pathogens affecting avocados worldwide. Recent global population analyses of P. cinnamomi identified two panglobal clonal lineages named PcG1-A2 and PcG2-A2, both of A2 mating type. In California avocado orchards, P. cinnamomi populations were previously classified into two clades, A2 clade I and A2 clade II, with the latter likely introduced from Mexico. In this study, we conducted the genetic characterization of 125 isolates collected from avocado-producing regions of the United States and investigated their genetic relationships with previous populations from California and Mexico and with the two panglobal A2 clonal lineages using whole-genome resequencing. All isolates were estimated to be triploid based on nQuire. Phylogenetic reconstruction and fastSTRUCTURE analyses based on single nucleotide polymorphisms showed that the PcG1-A2 reference isolate clustered with the previously described California A2 clade I and with most U.S. isolates. In contrast, the PcG2-A2 reference isolate clustered with the California A2 clade II and with most Mexican isolates, supporting a Mexican origin for this lineage. Discriminant analysis of principal components, principal coordinate analysis, and minimum spanning networks further resolved two distinct groups of A2 isolates, reinforcing the presence of two clonal lineages in avocado orchards across the United States. Isolates were assigned to multilocus genotypes (MLGs), including one widespread MLG containing isolates from all sampled avocado-growing regions. Mexico exhibited the highest genetic diversity, although unique MLGs were detected at each location. These results clarify the genetic relationships among P. cinnamomi populations in avocado orchards across the United States and link the previously described California clades to the two panglobal lineages currently recognized. Our findings support a hypothesis of pathogen movement among avocado-producing regions and reveal localized subpopulations that may pose risks to the sustainability of the avocado industry. Continued monitoring of P. cinnamomi populations will be essential for developing effective PRR management strategies to increase avocado production and enhance the national industry’s profitability, competitivity, and marketability.