A 20-kb lineage-specific genomic region tames virulence in pathogenic amphidiploid Verticillium longisporum

Rebekka Harting; Jessica Starke; Harald Kusch; Stefanie Pöggeler; Isabel Maurus; Rabea Schlüter; Manuel Landesfeind; Ingo Bulla; Minou Nowrousian; Ronnie de Jonge; Gertrud Stahlhut; Katharina J. Hoff; Kathrin P. Aßhauer; Andrea Thürmer; Mario Stanke; Rolf Daniel; Burkhard Morgenstern; Bart P.H.J. Thomma; James W. Kronstad; Susanna A. Braus-Stromeyer; Gerhard H. Braus

doi:10.1111/mpp.13071

A 20-kb lineage-specific genomic region tames virulence in pathogenic amphidiploid Verticillium longisporum

Rebekka Harting
, Jessica Starke
, Harald Kusch
, Stefanie Pöggeler
, Isabel Maurus
, Rabea Schlüter
, Manuel Landesfeind
, Ingo Bulla
, Minou Nowrousian
, Ronnie de Jonge
, Gertrud Stahlhut
, Katharina J. Hoff
, Kathrin P. Aßhauer
, Andrea Thürmer
, Mario Stanke
, Rolf Daniel
, Burkhard Morgenstern
, Bart P.H.J. Thomma
, James W. Kronstad
, Susanna A. Braus-Stromeyer

Gerhard H. Braus^*

^*Corresponding author for this work

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

11 Citations (Scopus)

Abstract

Amphidiploid fungal Verticillium longisporum strains Vl43 and Vl32 colonize the plant host Brassica napus but differ in their ability to cause disease symptoms. These strains represent two V. longisporum lineages derived from different hybridization events of haploid parental Verticillium strains. Vl32 and Vl43 carry same-sex mating-type genes derived from both parental lineages. Vl32 and Vl43 similarly colonize and penetrate plant roots, but asymptomatic Vl32 proliferation in planta is lower than virulent Vl43. The highly conserved Vl43 and Vl32 genomes include less than 1% unique genes, and the karyotypes of 15 or 16 chromosomes display changed genetic synteny due to substantial genomic reshuffling. A 20 kb Vl43 lineage-specific (LS) region apparently originating from the Verticillium dahliae-related ancestor is specific for symptomatic Vl43 and encodes seven genes, including two putative transcription factors. Either partial or complete deletion of this LS region in Vl43 did not reduce virulence but led to induction of even more severe disease symptoms in rapeseed. This suggests that the LS insertion in the genome of symptomatic V. longisporum Vl43 mediates virulence-reducing functions, limits damage on the host plant, and therefore tames Vl43 from being even more virulent.

Original language	English
Pages (from-to)	939-953
Journal	Molecular Plant Pathology
Volume	22
Issue number	8
Early online date	5 May 2021
DOIs	https://doi.org/10.1111/mpp.13071
Publication status	Published - Aug 2021

Keywords

genome comparison
hybridization
lineage-specific region
pathogenicity
Verticillium longisporum

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10.1111/mpp.13071Licence: CC BY-NC-ND

https://edepot.wur.nl/547722Licence: CC BY-NC-ND

Verticillium longisporum Vl43 genome sequencing and assembly
Harting, R. (Creator), Starke, J. (Creator), Kusch, H. (Creator), Pöggeler, S. (Creator), Maurus, I. (Creator), Schlüter, R. (Creator), Landesfeind, M. (Creator), Bulla, I. (Creator), Nowrousian, M. (Creator), de Jonge, R. (Creator), Stahlhut, G. (Creator), Hoff, K. J. (Creator), Aßhauer, K. P. (Creator), Thürmer, A. (Creator), Stanke, M. (Creator), Daniel, R. (Creator), Morgenstern, B. (Creator), Thomma, B. P. H. J. (Creator), Kronstad, J. W. (Creator), Braus-Stromeyer, S. A. (Creator) & Braus, G. H. (Creator), University of Göttingen, 22 Jun 2021
https://www.ncbi.nlm.nih.gov/bioproject/643983
Dataset
Verticillium longisporum strain:Vl32 Genome sequencing and assembly
Harting, R. (Creator), Starke, J. (Creator), Kusch, H. (Creator), Pöggeler, S. (Creator), Maurus, I. (Creator), Schlüter, R. (Creator), Landesfeind, M. (Creator), Bulla, I. (Creator), Nowrousian, M. (Creator), de Jonge, R. (Creator), Stahlhut, G. (Creator), Hoff, K. J. (Creator), Aßhauer, K. P. (Creator), Thürmer, A. (Creator), Stanke, M. (Creator), Daniel, R. (Creator), Morgenstern, B. (Creator), Thomma, B. P. H. J. (Creator), Kronstad, J. W. (Creator), Braus-Stromeyer, S. A. (Creator) & Braus, G. H. (Creator), University of Göttingen, 22 Jun 2021
https://www.ncbi.nlm.nih.gov/bioproject/643984
Dataset
Verticillium longisporum strain:Vl145c Genome sequencing and assembly
Harting, R. (Creator), Starke, J. (Creator), Kusch, H. (Creator), Pöggeler, S. (Creator), Maurus, I. (Creator), Schlüter, R. (Creator), Landesfeind, M. (Creator), Bulla, I. (Creator), Nowrousian, M. (Creator), de Jonge, R. (Creator), Stahlhut, G. (Creator), Hoff, K. J. (Creator), Aßhauer, K. P. (Creator), Thürmer, A. (Creator), Stanke, M. (Creator), Daniel, R. (Creator), Morgenstern, B. (Creator), Thomma, B. P. H. J. (Creator), Kronstad, J. W. (Creator), Braus-Stromeyer, S. A. (Creator) & Braus, G. H. (Creator), University of Göttingen, 3 Jun 2021
https://www.ncbi.nlm.nih.gov/bioproject/643985
Dataset

Cite this

Harting, R., Starke, J., Kusch, H., Pöggeler, S., Maurus, I., Schlüter, R., Landesfeind, M., Bulla, I., Nowrousian, M., de Jonge, R., Stahlhut, G., Hoff, K. J., Aßhauer, K. P., Thürmer, A., Stanke, M., Daniel, R., Morgenstern, B., Thomma, B. P. H. J., Kronstad, J. W., ... Braus, G. H. (2021). A 20-kb lineage-specific genomic region tames virulence in pathogenic amphidiploid Verticillium longisporum. Molecular Plant Pathology, 22(8), 939-953. https://doi.org/10.1111/mpp.13071

@article{dbc9ed8628b94ac1afe71ff0f47b67bc,

title = "A 20-kb lineage-specific genomic region tames virulence in pathogenic amphidiploid Verticillium longisporum",

abstract = "Amphidiploid fungal Verticillium longisporum strains Vl43 and Vl32 colonize the plant host Brassica napus but differ in their ability to cause disease symptoms. These strains represent two V. longisporum lineages derived from different hybridization events of haploid parental Verticillium strains. Vl32 and Vl43 carry same-sex mating-type genes derived from both parental lineages. Vl32 and Vl43 similarly colonize and penetrate plant roots, but asymptomatic Vl32 proliferation in planta is lower than virulent Vl43. The highly conserved Vl43 and Vl32 genomes include less than 1\% unique genes, and the karyotypes of 15 or 16 chromosomes display changed genetic synteny due to substantial genomic reshuffling. A 20 kb Vl43 lineage-specific (LS) region apparently originating from the Verticillium dahliae-related ancestor is specific for symptomatic Vl43 and encodes seven genes, including two putative transcription factors. Either partial or complete deletion of this LS region in Vl43 did not reduce virulence but led to induction of even more severe disease symptoms in rapeseed. This suggests that the LS insertion in the genome of symptomatic V. longisporum Vl43 mediates virulence-reducing functions, limits damage on the host plant, and therefore tames Vl43 from being even more virulent.",

keywords = "genome comparison, hybridization, lineage-specific region, pathogenicity, Verticillium longisporum",

author = "Rebekka Harting and Jessica Starke and Harald Kusch and Stefanie P{\"o}ggeler and Isabel Maurus and Rabea Schl{\"u}ter and Manuel Landesfeind and Ingo Bulla and Minou Nowrousian and \{de Jonge\}, Ronnie and Gertrud Stahlhut and Hoff, \{Katharina J.\} and A{\ss}hauer, \{Kathrin P.\} and Andrea Th{\"u}rmer and Mario Stanke and Rolf Daniel and Burkhard Morgenstern and Thomma, \{Bart P.H.J.\} and Kronstad, \{James W.\} and Braus-Stromeyer, \{Susanna A.\} and Braus, \{Gerhard H.\}",

year = "2021",

month = aug,

doi = "10.1111/mpp.13071",

language = "English",

volume = "22",

pages = "939--953",

journal = "Molecular Plant Pathology",

issn = "1464-6722",

publisher = "Wiley",

number = "8",

}

Harting, R, Starke, J, Kusch, H, Pöggeler, S, Maurus, I, Schlüter, R, Landesfeind, M, Bulla, I, Nowrousian, M, de Jonge, R, Stahlhut, G, Hoff, KJ, Aßhauer, KP, Thürmer, A, Stanke, M, Daniel, R, Morgenstern, B, Thomma, BPHJ, Kronstad, JW, Braus-Stromeyer, SA & Braus, GH 2021, 'A 20-kb lineage-specific genomic region tames virulence in pathogenic amphidiploid Verticillium longisporum', Molecular Plant Pathology, vol. 22, no. 8, pp. 939-953. https://doi.org/10.1111/mpp.13071

TY - JOUR

T1 - A 20-kb lineage-specific genomic region tames virulence in pathogenic amphidiploid Verticillium longisporum

AU - Harting, Rebekka

AU - Starke, Jessica

AU - Kusch, Harald

AU - Pöggeler, Stefanie

AU - Maurus, Isabel

AU - Schlüter, Rabea

AU - Landesfeind, Manuel

AU - Bulla, Ingo

AU - Nowrousian, Minou

AU - de Jonge, Ronnie

AU - Stahlhut, Gertrud

AU - Hoff, Katharina J.

AU - Aßhauer, Kathrin P.

AU - Thürmer, Andrea

AU - Stanke, Mario

AU - Daniel, Rolf

AU - Morgenstern, Burkhard

AU - Thomma, Bart P.H.J.

AU - Kronstad, James W.

AU - Braus-Stromeyer, Susanna A.

AU - Braus, Gerhard H.

PY - 2021/8

Y1 - 2021/8

N2 - Amphidiploid fungal Verticillium longisporum strains Vl43 and Vl32 colonize the plant host Brassica napus but differ in their ability to cause disease symptoms. These strains represent two V. longisporum lineages derived from different hybridization events of haploid parental Verticillium strains. Vl32 and Vl43 carry same-sex mating-type genes derived from both parental lineages. Vl32 and Vl43 similarly colonize and penetrate plant roots, but asymptomatic Vl32 proliferation in planta is lower than virulent Vl43. The highly conserved Vl43 and Vl32 genomes include less than 1% unique genes, and the karyotypes of 15 or 16 chromosomes display changed genetic synteny due to substantial genomic reshuffling. A 20 kb Vl43 lineage-specific (LS) region apparently originating from the Verticillium dahliae-related ancestor is specific for symptomatic Vl43 and encodes seven genes, including two putative transcription factors. Either partial or complete deletion of this LS region in Vl43 did not reduce virulence but led to induction of even more severe disease symptoms in rapeseed. This suggests that the LS insertion in the genome of symptomatic V. longisporum Vl43 mediates virulence-reducing functions, limits damage on the host plant, and therefore tames Vl43 from being even more virulent.

AB - Amphidiploid fungal Verticillium longisporum strains Vl43 and Vl32 colonize the plant host Brassica napus but differ in their ability to cause disease symptoms. These strains represent two V. longisporum lineages derived from different hybridization events of haploid parental Verticillium strains. Vl32 and Vl43 carry same-sex mating-type genes derived from both parental lineages. Vl32 and Vl43 similarly colonize and penetrate plant roots, but asymptomatic Vl32 proliferation in planta is lower than virulent Vl43. The highly conserved Vl43 and Vl32 genomes include less than 1% unique genes, and the karyotypes of 15 or 16 chromosomes display changed genetic synteny due to substantial genomic reshuffling. A 20 kb Vl43 lineage-specific (LS) region apparently originating from the Verticillium dahliae-related ancestor is specific for symptomatic Vl43 and encodes seven genes, including two putative transcription factors. Either partial or complete deletion of this LS region in Vl43 did not reduce virulence but led to induction of even more severe disease symptoms in rapeseed. This suggests that the LS insertion in the genome of symptomatic V. longisporum Vl43 mediates virulence-reducing functions, limits damage on the host plant, and therefore tames Vl43 from being even more virulent.

KW - genome comparison

KW - hybridization

KW - lineage-specific region

KW - pathogenicity

KW - Verticillium longisporum

U2 - 10.1111/mpp.13071

DO - 10.1111/mpp.13071

M3 - Article

AN - SCOPUS:85105180109

SN - 1464-6722

VL - 22

SP - 939

EP - 953

JO - Molecular Plant Pathology

JF - Molecular Plant Pathology

IS - 8

ER -

A 20-kb lineage-specific genomic region tames virulence in pathogenic amphidiploid Verticillium longisporum

Abstract

Keywords

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Datasets

Verticillium longisporum Vl43 genome sequencing and assembly

Verticillium longisporum strain:Vl32 Genome sequencing and assembly

Verticillium longisporum strain:Vl145c Genome sequencing and assembly

Cite this