Phylogeography and population structure of the global, wide host-range hybrid pathogen Phytophthora x cambivora

Authors: MULLETT, MARTIN - Mendel University; VAN POUCKE, KRIS - Institute For Agricultural And Fisheries Research (ILVO); HAEGEMAN, A - Flanders Research Institute For Agriculture; FOCQUET, F - Flanders Research Institute For Agriculture; CAULDRON, N - Oregon State University; KNAUS, BRIAN - Oregon State University; HORTA JUNG, MARILIA - Tokyo Metropolitan Agricultural And Forestry Research Center; KAGEYAMA, KOJI - Tokyo University Of Agriculture & Technology; HIENO, AYAKA - Forest Research; MASUJA, HAYATO - Eotvos Lorand University; UEMATSU, SEIJI - Tokyo University Of Agriculture & Technology; WEBBER, JOAN - Forest Research; BRASIER, CLIVE - Forest Research; BAKONYI, JOSZEF - Eotvos Lorand University; HEUNGENS, KURT - Institute For Agricultural And Fisheries Research (ILVO); Grunwald, Niklaus - Nik; JUNG, THOMAS - Mendel University

Submitted to: IMA Fungus
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/8/2023
Publication Date: 2/23/2023
Citation: Mullett, M., Van Poucke, K., Haegeman, A., Focquet, F., Cauldron, N., Knaus, B., Horta Jung, M., Kageyama, K., Hieno, A., Masuja, H., Uematsu, S., Webber, J., Brasier, C.M., Bakonyi, J., Heungens, K., Grunwald, N.J., Jung, T. 2023. Phylogeography and population structure of the global, wide host-range hybrid pathogen Phytophthora x cambivora. IMA Fungus. 14. Article 4. https://doi.org/10.1186/s43008-023-00109-6.
DOI: https://doi.org/10.1186/s43008-023-00109-6

Interpretive Summary: Invasive plant pathogens pose a major threat to native and agricultural ecosystems. The water mold Phytophthora ×cambivora is an invasive, destructive pathogen of forest and fruit trees causing severe damage worldwide to chestnuts, apricots, peaches, plums, almonds and cherries, apples, oaks, and beech. This pathogen was one of the first invasive Phytophthora pathogens to be introduced to Europe and North America. However, the origin of this pathogen remains unknown. We characterized populations from Europe, North and South America, Australia and East Asia using genetic approaches. Populations in North America, Europe and Australia are clonal (e.g. lack sex), whereas those in East Asia are predominantly sexual. Isolates from some fruit trees belong to a separate lineage found in Australia, North America, Europe and East Asia, indicating the disease on fruit trees. The highest genetic diversity was found in Japan, suggesting that East Asia is the center of origin of the pathogen, although further surveys in unsampled, temperate regions of East Asia are needed to identify the exact location and range of the center of diversity.

Technical Abstract: Invasive, exotic plant pathogens pose a major threat to native and agricultural ecosystems. Phytophthora ×cambivora is an invasive, destructive pathogen of forest and fruit trees causing severe damage worldwide to chestnuts (Castanea), apricots, peaches, plums, almonds and cherries (Prunus), apples (Malus), oaks (Quercus), and beech (Fagus). It was one of the first invasive Phytophthora species to be introduced to Europe and North America, although its origin is unknown. We determined the population genetic history in Europe, North and South America, Australia and East Asia using genotyping-by-sequencing. Populations in Europe and Australia appear clonal, while those in North America are highly clonal yet show some degree of sexual reproduction, whereas those in East Asia are predominantly sexual. Two clonal lineages, each of opposite mating type, and a hybrid lineage derived from these two lineages, dominated the populations in Europe and were predominantly found on sadfasdfasdfdfgdsgdfagaceous forest hosts (Castanea, Quercus, Fagus). Isolates from fruit trees (Prunus and Malus) belonged to a separate lineage found in Australia, North America, Europe and East Asia, indicating the disease on fruit trees could be caused by a distinct lineage of P. ×cambivora, which may potentially be a separate sister species and likely has been moved with live plants. The highest genetic diversity was found in Japan, suggesting that East Asia is the centre of origin of the pathogen, although further surveys in unsampled, temperate regions of East Asia are needed to identify the exact location and range of the centre of diversity.