Comparative genomic analysis of 31 Phytophthora genomes reveals genome plasticity and horizontal gene transfer

Authors: KRONMILLER, BRENT - Oregon State University; FEAU, NICOLAS - University Of British Columbia; SHEN, DANYU - Nanjing Agricultural University; TABIMA, JAVIER - Clark University; ALI, SHAHIN - US Department Of Agriculture (USDA); ARMITAGE, ANDREW - University Of Greenwich; ARREDONDO, FELIPE - Oregon State University; Bailey, Bryan; BOLLMANN, STEPHANIE - Oregon State University; DALE, ANGELA - University Of British Columbia; HARRISON, RICHARD - University Of Greenwich; HRYWKIW, KELLY - University Of British Columbia; Kasuga, Takao; MCDOUGAL, REBECCA - New Zealand Forest Research Institute; NELLIST, CHARLOTTE - University Of Greenwich; PANDA, PREETI - New Zealand Forest Research Institute; TRIPATHY, SUCHETA - Council Of Scientific And Industrial Research (CSIR); WILLIAMS, NARI - New Zealand Forest Research Institute; YE, WENWU - Nanjing Agricultural University; WANG, YUANCHAO - Nanjing Agricultural University; HAMELIN, RICHARD - University Of British Columbia; Grunwald, Niklaus - Nik

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/24/2022
Publication Date: 1/1/2023
Citation: Kronmiller, B.A., Feau, N., Shen, D., Tabima, J.F., Ali, S.S., Armitage, A.D., Arredondo, F., Bailey, B.A., Bollmann, S.R., Dale, A., Harrison, R., Hrywkiw, K., Kasuga, T., Mcdougal, R., Nellist, C.F., Panda, P., Tripathy, S., Williams, N.M., Ye, W., Wang, Y., Hamelin, R.C., Grunwald, N.J. 2023. Comparative genomic analysis of 31 Phytophthora genomes reveals genome plasticity and horizontal gene transfer. Molecular Plant-Microbe Interactions. 36:26-46. https://doi.org/10.1094/MPMI-06-22-0133-R.
DOI: https://doi.org/10.1094/MPMI-06-22-0133-R

Interpretive Summary: Phytophthora species are oomycete plant pathogens that cause great economic impact. The Phytophthora genus infects a wide range of plant hosts including crops, trees, and ornamentals. There are over 180 known Phytophthora species, we sequenced 31 individual Phytophthora species genomes and 24 samples of expressed genes to study genetic relationships across the genus. We showed a range of genome sizes, amounts of predicted genes, and repetitive content across the Phytophthora genus. Amounts of predicted pathogenicity-related genes varied across Phytophthora species and some of them increased as the host range of Phytophthora species increased. We also identified genes derived from bacteria and fungi in Phytophthora genomes. We conclude that the 31 genomes presented here are essential for investigating genus-wide genomic associations in Phytophthora.

Technical Abstract: Phytophthora species are oomycete plant pathogens that cause great economic impact. The Phytophthora genus infects a wide range of plant hosts including crops, trees, and ornamentals. There are over 180 known Phytophthora species, we sequenced 31 individual Phytophthora species genomes and 24 individual transcriptomes to study genetic relationships across the genus. De novo genome assemblies showed a range of genome sizes, amounts of predicted genes, and repetitive content across the Phytophthora genus. A genus-wide orthology was created to evaluate orthologous groups of genes. Amounts of predicted effector genes varied across Phytophthora species by type of effector, genome size, and also the plant host range. Predicted amounts of appoplastic effectors increased as the host range of Phytophthora species increased. Predicted amounts of cytoplasmic effectors also increased with host range but leveled off or decreased in Phytophthora that have enormous host ranges. With extensive sequencing across the Phytophthora genus we now have the genomic resources to evaluate horizontal gene transfer events across the oomycetes. Using a machine learning approach to identify horizontally transferred genes from bacterial and fungal origin we identified 44 candidates in Phytophthora species. Phylogenetic reconstruction shows that the transfers of most of the 44 candidates happened in parallel to major progresses in the development of the Phytophthora genus. We conclude that the 31 genomes presented here are essential for investigating genus-wide genomic associations in Phytophthora.