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

Anouk C van Westerhoven; Carolina Aguilera-Galvez; Giuliana Nakasato-Tagami; Xiaoqian Shi-Kunne; Einar Martinez de la Parte; Edgar Chavarro-Carrero; Harold J G Meijer; Alice Feurtey; Nani Maryani; Nadia Ordóñez; Harrie Schneiders; Koen Nijbroek; Alexander H J Wittenberg; Rene Hofstede; Fernando García-Bastidas; Anker Sørensen; Ronny Swennen; Andre Drenth; Eva H Stukenbrock; Gert H J Kema; Michael F Seidl

doi:10.1111/nph.19604

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

Anouk C van Westerhoven, Carolina Aguilera-Galvez, Giuliana Nakasato-Tagami, Xiaoqian Shi-Kunne, Einar Martinez de la Parte, Edgar Chavarro-Carrero, Harold J G Meijer, Alice Feurtey, Nani Maryani, Nadia Ordóñez, Harrie Schneiders, Koen Nijbroek, Alexander H J Wittenberg, Rene Hofstede, Fernando García-Bastidas, Anker Sørensen, Ronny Swennen, Andre Drenth, Eva H Stukenbrock, Gert H J Kema^*Michael F Seidl^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

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.

Original language	English
Pages (from-to)	610-625
Number of pages	16
Journal	The New phytologist
Volume	242
Issue number	2
Early online date	25 Feb 2024
DOIs	https://doi.org/10.1111/nph.19604
Publication status	Published - Apr 2024

Bibliographical note

Publisher Copyright:
© 2024 The Authors. New Phytologist © 2024 New Phytologist Foundation.

Funding

ACW, GHJK, CAG, GNT, RS, and JD were supported by the Bill and Melinda Gates Foundation, grant no.: AG ‐ 4425. Banana research at Wageningen University has been supported by the Dutch Dioraphte Foundation, grant no.: 20 04 04 02. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank the Research Support Group (RSG) at KeyGene (Wageningen, the Netherlands), which provided DNA isolation, library preparation, and long‐read sequencing for three of the strains.

Funders	Funder number
Dutch Dioraphte Foundation	20 04 04 02
Bill and Melinda Gates Foundation	AG ‐ 4425

Keywords

Fusarium oxysporum
accessory regions
genome compartmentalization
pathogen genome evolution
segmental duplications

Access to Document

10.1111/nph.19604Licence: CC BY

New Phytologist - 2024 - Westerhoven - Segmental duplications drive the evolution of accessory regions in a major cropFinal published version, 6.71 MBLicence: CC BY

Cite this

van Westerhoven, A. C., Aguilera-Galvez, C., Nakasato-Tagami, G., Shi-Kunne, X., Martinez de la Parte, E., Chavarro-Carrero, E., Meijer, H. J. G., Feurtey, A., Maryani, N., Ordóñez, N., Schneiders, H., Nijbroek, K., Wittenberg, A. H. J., Hofstede, R., García-Bastidas, F., Sørensen, A., Swennen, R., Drenth, A., Stukenbrock, E. H., ... Seidl, M. F. (2024). Segmental duplications drive the evolution of accessory regions in a major crop pathogen. The New phytologist, 242(2), 610-625. https://doi.org/10.1111/nph.19604

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abstract = "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.",

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note = "Publisher Copyright: {\textcopyright} 2024 The Authors. New Phytologist {\textcopyright} 2024 New Phytologist Foundation.",

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month = apr,

doi = "10.1111/nph.19604",

language = "English",

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van Westerhoven, AC, Aguilera-Galvez, C, Nakasato-Tagami, G, Shi-Kunne, X, Martinez de la Parte, E, Chavarro-Carrero, E, Meijer, HJG, Feurtey, A, Maryani, N, Ordóñez, N, Schneiders, H, Nijbroek, K, Wittenberg, AHJ, Hofstede, R, García-Bastidas, F, Sørensen, A, Swennen, R, Drenth, A, Stukenbrock, EH, Kema, GHJ & Seidl, MF 2024, 'Segmental duplications drive the evolution of accessory regions in a major crop pathogen', The New phytologist, vol. 242, no. 2, pp. 610-625. https://doi.org/10.1111/nph.19604

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AU - Ordóñez, Nadia

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AU - García-Bastidas, Fernando

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AU - Swennen, Ronny

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

Abstract

Bibliographical note

Funding

Keywords

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