Intraspecific variation and recent loss of ancient, conserved effector genes in the sudden oak death pathogen Phytophthora ramorum

Authors: CAULDRON, NICHOLAS - Oregon State University; Press, Caroline; WEISBERG, ALEXANDRA - Oregon State University; HORTA JUNG, MARÍLIA - Mendel University; CORCOBADO, TAMARA - Mendel University; WEBBER, JOAN - Forest Research; KAGEYAMA, KOJI - Gifu University; HIENO, AYAKA - Gifu University; MASUYA, HAYATO - Forestry And Forest Products Research Institute (FFPRI); UEMATSU, SEIJI - Tokyo University Of Agriculture & Technology; SCANU, BRUNO - University Of Sassari; BRASIER, CLIVE - Forest Research; JUNG, THOMAS - Mendel University; CHANG, JEFF - Oregon State University; Grunwald, Niklaus

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/24/2025
Publication Date: 1/24/2025
Citation: Cauldron, N.C., Press, C.M., Weisberg, A.J., Horta Jung, M., Corcobado, T., Webber, J.F., Kageyama, K., Hieno, A., Masuya, H., Uematsu, S., Scanu, B., Brasier, C.M., Jung, T., Chang, J.H., Grunwald, N.J. 2025. Intraspecific variation and recent loss of ancient, conserved effector genes in the sudden oak death pathogen Phytophthora ramorum. Molecular Plant-Microbe Interactions. 38(3):440-453. https://doi.org/10.1094/MPMI-10-24-0131-R.
DOI: https://doi.org/10.1094/MPMI-10-24-0131-R

Interpretive Summary: Members of the plant pathogen genus Phytophthora are responsible for many important diseases of plants in agricultural and natural ecosystems. Phytophthora ramorum causes sudden oak death, a disease with devastating effects on oak and tanoak stands in western US forests. Multiple known genetic variants exist with differences in how they attack hosts; thus, understanding the genetics could lead to a better understanding of these observed differences. Recent discovery of P. ramorum in Asia provides a new opportunity for a deeper investigation of the genetic history of the species. We sequenced and analyzed the genomes of P. ramorum samples, including three from Asia and three representing variants causing epidemics in western US forests. The six genomes were assembled into 13 chromosomes. We characterized the evolution and inferred changes in genes to be important for infection of plant hosts. We observed large changes in some genes. These results provide novel insights into the evolution and adaptation of the sudden oak death pathogen.

Technical Abstract: Members of the Phytophthora genus are responsible for many important diseases of plants in agricultural and natural ecosystems. Phytophthora ramorum causes devastating diseases of oak and tanoak stands in western US forests and in larch plantations in the UK. The four evolutionary lineages involved express different virulence phenotypes on plant hosts, and characterization of gene content is foundational to understanding the basis for these differences. Recent discovery of P. ramorum at its candidate center of origin in Asia provides a new opportunity for investigating the evolutionary history of the species. We assembled, high-quality genome sequences of six P. ramorum isolates representing three lineages from Asia and three causing epidemics in western US forests. The six genomes were assembled into 13 putative chromosomes. Analysis of structural variation revealed multiple chromosome fusion and fission events. Analysis of putative virulence genes revealed variations in effector gene composition among the sequenced lineages. We further characterized their evolutionary history and inferred a contraction of crinkler-encoding genes in the subclade of Phytophthora containing P. ramorum. There were losses of multiple families and a near complete loss of paralogs in the largest core crinkler family in the ancestor of P. ramorum and sister species P. lateralis. Surprisingly, within P. ramorum, the degree of variation in abundance of genes predicted to encode secreted glycoside hydrolase enzymes is equivalent to that observed among species of Phytophthora. We found plasticity among genomes from multiple lineages in a Phytophthora species and provide insights into the evolutionary history of a class of anciently conserved effector genes.