Comparative Genomic Analysis of 31 Phytophthora Genomes Reveals Genome Plasticity and Horizontal Gene Transfer

Author:

Kronmiller Brent A.12ORCID,Feau Nicolas3,Shen Danyu4,Tabima Javier F.5,Ali Shahin S.6,Armitage Andrew D.7,Arredondo Felipe12,Bailey Bryan A.6,Bollmann Stephanie R.8,Dale Angela39,Harrison Richard J.10,Hrywkiw Kelly3,Kasuga Takao11,McDougal Rebecca12,Nellist Charlotte F.10,Panda Preeti13,Tripathy Sucheta14,Williams Nari M.1215,Ye Wenwu4ORCID,Wang Yuanchao4,Hamelin Richard C.31617,Grünwald Niklaus J.18ORCID

Affiliation:

1. Center for Quantitative Life Sciences, Oregon State University, Corvallis, OR, U.S.A.

2. Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, U.S.A.

3. Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, Canada

4. Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China

5. Department of Biology, Clark University, Worcester, MA, U.S.A.

6. Sustainable Perennial Crops Laboratory, Northeast Area, USDA/ARS, Beltsville Agricultural Research Center-West, Beltsville, MD, U.S.A.

7. Natural Resources Institute, University of Greenwich, Chatham Maritime, U.K.

8. Department of Integrative Biology, Oregon State University, Corvallis, OR, U.S.A.

9. SC-New Construction Materials, FPInnovations, Vancouver, V6T 1Z4, Canada

10. NIAB EMR, East Malling, U.K.

11. Crops Pathology and Genetics Research Unit, Agricultural Research Service, United States Department of Agriculture, Davis, CA, U.S.A.

12. Scion (Zealand Forest Research Institute), 49 Sala Street, Te Papa Tipu Innovation Park, Private Bag 3020, Rotorua, New Zealand

13. The New Zealand Institute for Plant and Food Research Ltd, 74 Gerald Street, Lincoln, 7608, New Zealand

14. CSIR Indian Institute of Chemical Biology, Kolkata, India

15. Department of Pathogen Ecology and Control, Plant and Food Research, Private Bag 1401, Havelock North, New Zealand

16. Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec, Canada

17. Département des sciences du bois et de la forêt, Faculté de Foresterie et Géographie, Université Laval, Québec, Canada

18. Horticultural Crop Research Unit, United States Department of Agriculture, Agricultural Research Service, Corvallis, OR, U.S.A.

Abstract

Phytophthora species are oomycete plant pathogens that cause great economic and ecological impacts. The Phytophthora genus includes over 180 known species, infecting a wide range of plant hosts, including crops, trees, and ornamentals. We sequenced the genomes of 31 individual Phytophthora species and 24 individual transcriptomes to study genetic relationships across the genus. De novo genome assemblies revealed variation in genome sizes, numbers of predicted genes, and in repetitive element content across the Phytophthora genus. A genus-wide comparison evaluated orthologous groups of genes. Predicted effector gene counts varied across Phytophthora species by effector family, genome size, and plant host range. Predicted numbers of apoplastic effectors increased as the host range of Phytophthora species increased. Predicted numbers of cytoplasmic effectors also increased with host range but leveled off or decreased in Phytophthora species 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 with bacterial or fungal origin, we identified 44 candidates over 36 Phytophthora species genomes. Phylogenetic reconstruction indicates that the transfers of most of these 44 candidates happened in parallel to major advances in the evolution of the oomycetes and Phytophthora spp. We conclude that the 31 genomes presented here are essential for investigating genus-wide genomic associations in genus Phytophthora. [Formula: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .

Funder

China National Funds for Distinguished Young Scientists

California Walnut Board

United States Department of Agriculture Agriculture Research Service

United States Department of Agriculture National Institute of Food and Agriculture

J Frank Schmidt Foundation

U.K. Biotechnology and Biological Sciences Research Council

New Zealand Ministry of Business, Innovation and Employment

Forest Growers Levy Trust

Radiata Pine Breeding Company

Publisher

Scientific Societies

Subject

Agronomy and Crop Science,General Medicine,Physiology

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