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

13 Citations (Scopus)

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
Journal	New Phytologist
Volume	242
Issue number	2
Early online date	25 Feb 2024
DOIs	https://doi.org/10.1111/nph.19604
Publication status	Published - 2024

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https://edepot.wur.nl/651371Licence: CC BY

Fusarium oxysporum f. sp. cubense Genome sequencing and assembly
van Westerhoven, A. C. (Creator), Aguilera‐Galvez, C. (Creator), Nakasato‐Tagami, G. (Creator), Shi‐Kunne, X. (Creator), Martinez de la Parte, E. (Creator), Chavarro‐Carrero, E. (Creator), Meijer, H. J. G. (Creator), Feurtey, A. (Creator), Maryani, N. (Creator), Ordóñez, N. (Creator), Schneiders, H. (Creator), Nijbroek, K. (Creator), Wittenberg, A. H. J. (Creator), Hofstede, R. (Creator), García‐Bastidas, F. (Creator), Sørensen, A. (Creator), Swennen, R. (Creator), Drenth, A. (Creator), Stukenbrock, E. H. (Creator), Kema, G. H. J. (Creator) & Seidl, M. F. (Creator), Wageningen University & Research, 5 Jun 2023
https://www.ncbi.nlm.nih.gov/bioproject/979975
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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. New Phytologist, 242(2), 610-625. https://doi.org/10.1111/nph.19604

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title = "Segmental duplications drive the evolution of accessory regions in a major crop pathogen",

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.",

author = "{van Westerhoven}, {Anouk C.} and Carolina Aguilera‐Galvez and Giuliana Nakasato‐Tagami and Xiaoqian Shi‐Kunne and {Martinez de la Parte}, Einar and Edgar Chavarro‐Carrero and Meijer, {Harold J.G.} and Alice Feurtey and Nani Maryani and Nadia Ord{\'o}{\~n}ez and Harrie Schneiders and Koen Nijbroek and Wittenberg, {Alexander H.J.} and Rene Hofstede and Fernando Garc{\'i}a‐Bastidas and Anker S{\o}rensen and Ronny Swennen and Andre Drenth and Stukenbrock, {Eva H.} and Kema, {Gert H.J.} and Seidl, {Michael F.}",

year = "2024",

doi = "10.1111/nph.19604",

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journal = "New Phytologist",

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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', New Phytologist, vol. 242, no. 2, pp. 610-625. https://doi.org/10.1111/nph.19604

TY - JOUR

T1 - Segmental duplications drive the evolution of accessory regions in a major crop pathogen

AU - van Westerhoven, Anouk C.

AU - Aguilera‐Galvez, Carolina

AU - Nakasato‐Tagami, Giuliana

AU - Shi‐Kunne, Xiaoqian

AU - Martinez de la Parte, Einar

AU - Chavarro‐Carrero, Edgar

AU - Meijer, Harold J.G.

AU - Feurtey, Alice

AU - Maryani, Nani

AU - Ordóñez, Nadia

AU - Schneiders, Harrie

AU - Nijbroek, Koen

AU - Wittenberg, Alexander H.J.

AU - Hofstede, Rene

AU - García‐Bastidas, Fernando

AU - Sørensen, Anker

AU - Swennen, Ronny

AU - Drenth, Andre

AU - Stukenbrock, Eva H.

AU - Kema, Gert H.J.

AU - Seidl, Michael F.

PY - 2024

Y1 - 2024

N2 - 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.

AB - 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.

U2 - 10.1111/nph.19604

DO - 10.1111/nph.19604

M3 - Article

SN - 0028-646X

VL - 242

SP - 610

EP - 625

JO - New Phytologist

JF - New Phytologist

IS - 2

ER -

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

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Fusarium oxysporum f. sp. cubense Genome sequencing and assembly

Cite this