Segmental duplications drive the evolution of accessory regions in a major crop pathogen

Author:

van Westerhoven Anouk C.12ORCID,Aguilera‐Galvez Carolina1ORCID,Nakasato‐Tagami Giuliana1ORCID,Shi‐Kunne Xiaoqian1ORCID,Martinez de la Parte Einar1ORCID,Chavarro‐Carrero Edgar1ORCID,Meijer Harold J. G.13ORCID,Feurtey Alice456ORCID,Maryani Nani7ORCID,Ordóñez Nadia1ORCID,Schneiders Harrie8,Nijbroek Koen8,Wittenberg Alexander H. J.8,Hofstede Rene8,García‐Bastidas Fernando8ORCID,Sørensen Anker8,Swennen Ronny910ORCID,Drenth Andre11ORCID,Stukenbrock Eva H.45ORCID,Kema Gert H. J.1ORCID,Seidl Michael F.2ORCID

Affiliation:

1. Laboratory of Phytopathology Wageningen University Droevendaalsesteeg 1 6708 PB Wageningen the Netherlands

2. Department of Biology, Theoretical Biology & Bioinformatics Utrecht University Padualaan 8 3584 CH Utrecht the Netherlands

3. Department Biointeractions and Plant Health Wageningen University Droevendaalsesteeg 1 6708 PB Wageningen the Netherlands

4. Christian‐Albrechts University of Kiel Christian‐Albrechts‐Platz 4 24118 Kiel Germany

5. Max Planck Institute for Evolutionary Biology August‐Thienemann‐Straße 2 24306 Plön Germany

6. Plant Pathology Eidgenössische Technische Hochschule Zürich Rämistrasse 101 8092 Zürich Switzerland

7. Biology Education Universitas Sultan Ageng Tirtayasa Jalan Raya Palka No.Km 3 42163 Banten Indonesia

8. KeyGene Agro Business Park 90 6708 PW Wageningen the Netherlands

9. Division of Crop Biotechnics, Laboratory of Tropical Crop Improvement Catholic University of Leuven Oude Markt 13 3000 Leuven Belgium

10. International Institute of Tropical Agriculture Plot 15 Naguru E Rd Kampala PO Box 7878 Uganda

11. The University of Queensland St Lucia 4072 Brisbane Queensland Australia

Abstract

Summary Many pathogens evolved compartmentalized genomes with conserved core and variable accessory regions (ARs) that carry effector genes mediating virulence. The fungal plant pathogen Fusarium oxysporum has such ARs, often spanning entire chromosomes. The presence of specific ARs influences the host range, and horizontal transfer of ARs can modify the pathogenicity of the receiving strain. However, how these ARs evolve in strains that infect the same host remains largely unknown. We defined the pan‐genome of 69 diverse F. oxysporum strains that cause Fusarium wilt of banana, a significant constraint to global banana production, and analyzed the diversity and evolution of the ARs. Accessory regions in F. oxysporum strains infecting the same banana cultivar are highly diverse, and we could not identify any shared genomic regions and in planta‐induced effectors. We demonstrate that segmental duplications drive the evolution of ARs. Furthermore, we show that recent segmental duplications specifically in accessory chromosomes cause the expansion of ARs in F. oxysporum. Taken together, we conclude that extensive recent duplications drive the evolution of ARs in F. oxysporum, which contribute to the evolution of virulence.

Funder

Bill and Melinda Gates Foundation

Stichting Dioraphte

Publisher

Wiley

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