Functional analyses of small secreted cysteine‐rich proteins identified candidate effectors in Verticillium dahliae
Secreted small cysteine‐rich proteins (SCPs) play a critical role in modulating host immunity in plant–pathogen interactions. Bioinformatic analyses showed that the fungal pathogen Verticillium dahliae encodes more than 100 VdSCPs, but their roles in host–pathogen interactions have not been fully ch...
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Published in | Molecular plant pathology Vol. 21; no. 5; pp. 667 - 685 |
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Main Authors | , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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England
John Wiley & Sons, Inc
01.05.2020
John Wiley and Sons Inc |
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Abstract | Secreted small cysteine‐rich proteins (SCPs) play a critical role in modulating host immunity in plant–pathogen interactions. Bioinformatic analyses showed that the fungal pathogen Verticillium dahliae encodes more than 100 VdSCPs, but their roles in host–pathogen interactions have not been fully characterized. Transient expression of 123 VdSCP‐encoding genes in Nicotiana benthamiana identified three candidate genes involved in host–pathogen interactions. The expression of these three proteins, VdSCP27, VdSCP113, and VdSCP126, in N. benthamiana resulted in cell death accompanied by a reactive oxygen species burst, callose deposition, and induction of defence genes. The three VdSCPs mainly localized to the periphery of the cell. BAK1 and SOBIR1 (associated with receptor‐like protein) were required for the immunity triggered by these three VdSCPs in N. benthamiana. Site‐directed mutagenesis showed that cysteine residues that form disulphide bonds are essential for the functioning of VdSCP126, but not VdSCP27 and VdSCP113. VdSCP27, VdSCP113, and VdSCP126 individually are not essential for V. dahliae infection of N. benthamiana and Gossypium hirsutum, although there was a significant reduction of virulence on N. benthamiana and G. hirsutum when inoculated with the VdSCP27/VdSCP126 double deletion strain. These results illustrate that the SCPs play a critical role in the V. dahliae–plant interaction via an intrinsic virulence function and suppress immunity following infection.
Small cysteine‐rich proteins secreted by Verticillium dahliae play critical roles in interactions with hosts via an intrinsic virulence function and can suppress immunity following infection. |
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AbstractList | Abstract
Secreted small cysteine‐rich proteins (SCPs) play a critical role in modulating host immunity in plant–pathogen interactions. Bioinformatic analyses showed that the fungal pathogen
Verticillium dahliae
encodes more than 100 VdSCPs, but their roles in host–pathogen interactions have not been fully characterized. Transient expression of 123 VdSCP‐encoding genes in
Nicotiana benthamiana
identified three candidate genes involved in host–pathogen interactions. The expression of these three proteins, VdSCP27, VdSCP113, and VdSCP126, in
N. benthamiana
resulted in cell death accompanied by a reactive oxygen species burst, callose deposition, and induction of defence genes. The three VdSCPs mainly localized to the periphery of the cell. BAK1 and SOBIR1 (associated with receptor‐like protein) were required for the immunity triggered by these three VdSCPs in
N. benthamiana
. Site‐directed mutagenesis showed that cysteine residues that form disulphide bonds are essential for the functioning of VdSCP126, but not VdSCP27 and VdSCP113.
VdSCP27
,
VdSCP113
, and
VdSCP126
individually are not essential for
V. dahliae
infection of
N. benthamiana
and
Gossypium hirsutum
, although there was a significant reduction of virulence on
N. benthamiana
and
G. hirsutum
when inoculated with the
VdSCP27
/
VdSCP126
double deletion strain. These results illustrate that the SCPs play a critical role in the
V. dahliae–
plant interaction via an intrinsic virulence function and suppress immunity following infection. Secreted small cysteine‐rich proteins (SCPs) play a critical role in modulating host immunity in plant–pathogen interactions. Bioinformatic analyses showed that the fungal pathogen Verticillium dahliae encodes more than 100 VdSCPs, but their roles in host–pathogen interactions have not been fully characterized. Transient expression of 123 VdSCP‐encoding genes in Nicotiana benthamiana identified three candidate genes involved in host–pathogen interactions. The expression of these three proteins, VdSCP27, VdSCP113, and VdSCP126, in N. benthamiana resulted in cell death accompanied by a reactive oxygen species burst, callose deposition, and induction of defence genes. The three VdSCPs mainly localized to the periphery of the cell. BAK1 and SOBIR1 (associated with receptor‐like protein) were required for the immunity triggered by these three VdSCPs in N. benthamiana. Site‐directed mutagenesis showed that cysteine residues that form disulphide bonds are essential for the functioning of VdSCP126, but not VdSCP27 and VdSCP113. VdSCP27, VdSCP113, and VdSCP126 individually are not essential for V. dahliae infection of N. benthamiana and Gossypium hirsutum, although there was a significant reduction of virulence on N. benthamiana and G. hirsutum when inoculated with the VdSCP27/VdSCP126 double deletion strain. These results illustrate that the SCPs play a critical role in the V. dahliae–plant interaction via an intrinsic virulence function and suppress immunity following infection. Secreted small cysteine-rich proteins (SCPs) play a critical role in modulating host immunity in plant-pathogen interactions. Bioinformatic analyses showed that the fungal pathogen Verticillium dahliae encodes more than 100 VdSCPs, but their roles in host-pathogen interactions have not been fully characterized. Transient expression of 123 VdSCP-encoding genes in Nicotiana benthamiana identified three candidate genes involved in host-pathogen interactions. The expression of these three proteins, VdSCP27, VdSCP113, and VdSCP126, in N. benthamiana resulted in cell death accompanied by a reactive oxygen species burst, callose deposition, and induction of defence genes. The three VdSCPs mainly localized to the periphery of the cell. BAK1 and SOBIR1 (associated with receptor-like protein) were required for the immunity triggered by these three VdSCPs in N. benthamiana. Site-directed mutagenesis showed that cysteine residues that form disulphide bonds are essential for the functioning of VdSCP126, but not VdSCP27 and VdSCP113. VdSCP27, VdSCP113, and VdSCP126 individually are not essential for V. dahliae infection of N. benthamiana and Gossypium hirsutum, although there was a significant reduction of virulence on N. benthamiana and G. hirsutum when inoculated with the VdSCP27/VdSCP126 double deletion strain. These results illustrate that the SCPs play a critical role in the V. dahliae-plant interaction via an intrinsic virulence function and suppress immunity following infection. Secreted small cysteine‐rich proteins (SCPs) play a critical role in modulating host immunity in plant–pathogen interactions. Bioinformatic analyses showed that the fungal pathogen Verticillium dahliae encodes more than 100 VdSCPs, but their roles in host–pathogen interactions have not been fully characterized. Transient expression of 123 VdSCP‐encoding genes in Nicotiana benthamiana identified three candidate genes involved in host–pathogen interactions. The expression of these three proteins, VdSCP27, VdSCP113, and VdSCP126, in N. benthamiana resulted in cell death accompanied by a reactive oxygen species burst, callose deposition, and induction of defence genes. The three VdSCPs mainly localized to the periphery of the cell. BAK1 and SOBIR1 (associated with receptor‐like protein) were required for the immunity triggered by these three VdSCPs in N. benthamiana. Site‐directed mutagenesis showed that cysteine residues that form disulphide bonds are essential for the functioning of VdSCP126, but not VdSCP27 and VdSCP113. VdSCP27, VdSCP113, and VdSCP126 individually are not essential for V. dahliae infection of N. benthamiana and Gossypium hirsutum, although there was a significant reduction of virulence on N. benthamiana and G. hirsutum when inoculated with the VdSCP27/VdSCP126 double deletion strain. These results illustrate that the SCPs play a critical role in the V. dahliae–plant interaction via an intrinsic virulence function and suppress immunity following infection. Small cysteine‐rich proteins secreted by Verticillium dahliae play critical roles in interactions with hosts via an intrinsic virulence function and can suppress immunity following infection. Secreted small cysteine‐rich proteins (SCPs) play a critical role in modulating host immunity in plant–pathogen interactions. Bioinformatic analyses showed that the fungal pathogen Verticillium dahliae encodes more than 100 VdSCPs, but their roles in host–pathogen interactions have not been fully characterized. Transient expression of 123 VdSCP‐encoding genes in Nicotiana benthamiana identified three candidate genes involved in host–pathogen interactions. The expression of these three proteins, VdSCP27, VdSCP113, and VdSCP126, in N. benthamiana resulted in cell death accompanied by a reactive oxygen species burst, callose deposition, and induction of defence genes. The three VdSCPs mainly localized to the periphery of the cell. BAK1 and SOBIR1 (associated with receptor‐like protein) were required for the immunity triggered by these three VdSCPs in N. benthamiana . Site‐directed mutagenesis showed that cysteine residues that form disulphide bonds are essential for the functioning of VdSCP126, but not VdSCP27 and VdSCP113. VdSCP27 , VdSCP113 , and VdSCP126 individually are not essential for V. dahliae infection of N. benthamiana and Gossypium hirsutum , although there was a significant reduction of virulence on N. benthamiana and G. hirsutum when inoculated with the VdSCP27 / VdSCP126 double deletion strain. These results illustrate that the SCPs play a critical role in the V. dahliae– plant interaction via an intrinsic virulence function and suppress immunity following infection. Small cysteine‐rich proteins secreted by Verticillium dahliae play critical roles in interactions with hosts via an intrinsic virulence function and can suppress immunity following infection. |
Audience | Academic |
Author | Subbarao, Krishna V. Wang, Dan Kong, Zhi‐Qiang Tian, Li Dai, Xiao‐Feng Yin, Chun‐Mei Wang, Bao‐Li Song, Jian Wang, Jie Liu, Yan Zhou, Lei Li, Ting‐Gang Chen, Jie‐Yin Li, Jun‐Jiao Adamu, Sabiu Klosterman, Steven J. Song, Shuang‐Shuang Zhang, Dan‐Dan |
AuthorAffiliation | 2 Institute of Plant Protection Chinese Academy of Agricultural Sciences Beijing China 3 College of Life Science Qufu Normal University Qufu China 6 Department of Plant Pathology University of California Davis, c/o United States Agricultural Research Station Salinas CA USA 5 United States Department of Agriculture Agricultural Research Service Salinas CA USA 1 Laboratory of Cotton Disease Institute of Food Science and Technology Chinese Academy of Agricultural Sciences Beijing China 4 Key Laboratory of Agro‐products Quality and Safety Control in Storage and Transport Process Ministry of Agriculture Beijing China |
AuthorAffiliation_xml | – name: 1 Laboratory of Cotton Disease Institute of Food Science and Technology Chinese Academy of Agricultural Sciences Beijing China – name: 2 Institute of Plant Protection Chinese Academy of Agricultural Sciences Beijing China – name: 5 United States Department of Agriculture Agricultural Research Service Salinas CA USA – name: 6 Department of Plant Pathology University of California Davis, c/o United States Agricultural Research Station Salinas CA USA – name: 3 College of Life Science Qufu Normal University Qufu China – name: 4 Key Laboratory of Agro‐products Quality and Safety Control in Storage and Transport Process Ministry of Agriculture Beijing China |
Author_xml | – sequence: 1 givenname: Dan surname: Wang fullname: Wang, Dan organization: Chinese Academy of Agricultural Sciences – sequence: 2 givenname: Li surname: Tian fullname: Tian, Li organization: Qufu Normal University – sequence: 3 givenname: Dan‐Dan surname: Zhang fullname: Zhang, Dan‐Dan organization: Ministry of Agriculture – sequence: 4 givenname: Jian surname: Song fullname: Song, Jian organization: Chinese Academy of Agricultural Sciences – sequence: 5 givenname: Shuang‐Shuang surname: Song fullname: Song, Shuang‐Shuang organization: Qufu Normal University – sequence: 6 givenname: Chun‐Mei surname: Yin fullname: Yin, Chun‐Mei organization: Chinese Academy of Agricultural Sciences – sequence: 7 givenname: Lei surname: Zhou fullname: Zhou, Lei organization: Ministry of Agriculture – sequence: 8 givenname: Yan surname: Liu fullname: Liu, Yan organization: Qufu Normal University – sequence: 9 givenname: Bao‐Li surname: Wang fullname: Wang, Bao‐Li organization: Chinese Academy of Agricultural Sciences – sequence: 10 givenname: Zhi‐Qiang surname: Kong fullname: Kong, Zhi‐Qiang organization: Chinese Academy of Agricultural Sciences – sequence: 11 givenname: Steven J. surname: Klosterman fullname: Klosterman, Steven J. organization: Agricultural Research Service – sequence: 12 givenname: Jun‐Jiao surname: Li fullname: Li, Jun‐Jiao organization: Chinese Academy of Agricultural Sciences – sequence: 13 givenname: Jie surname: Wang fullname: Wang, Jie organization: Chinese Academy of Agricultural Sciences – sequence: 14 givenname: Ting‐Gang surname: Li fullname: Li, Ting‐Gang organization: Chinese Academy of Agricultural Sciences – sequence: 15 givenname: Sabiu surname: Adamu fullname: Adamu, Sabiu organization: Chinese Academy of Agricultural Sciences – sequence: 16 givenname: Krishna V. orcidid: 0000-0002-2075-1835 surname: Subbarao fullname: Subbarao, Krishna V. email: kvsubbarao@ucdavis.edu organization: Davis, c/o United States Agricultural Research Station – sequence: 17 givenname: Jie‐Yin orcidid: 0000-0002-8040-099X surname: Chen fullname: Chen, Jie‐Yin email: chenjieyin@caas.cn organization: Ministry of Agriculture – sequence: 18 givenname: Xiao‐Feng surname: Dai fullname: Dai, Xiao‐Feng email: daixiaofeng0002@126.com organization: Ministry of Agriculture |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32314529$$D View this record in MEDLINE/PubMed |
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Copyright | 2020 The Authors. published by British Society for Plant Pathology and John Wiley & Sons Ltd 2020 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd. COPYRIGHT 2020 John Wiley & Sons, Inc. 2020. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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Keywords | Verticillium dahliae virulence pathogen-associated molecular pattern (PAMPs) small cysteine-rich proteins (SCPs) effector immunity disulphide bonds |
Language | English |
License | Attribution 2020 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
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Notes | Funding information This work was supported by the Special Public Welfare Industry Research on Agriculture (201503109), the National Key Research and Development Program of China (2017YFD0201900, 2017YFD0200601), the Young Elite Scientists Sponsorship Program by CAST (2016QNRC001), the National Natural Science Foundation of China (31671986, 31471759, 31501588, 31772245, 31870138), an Agricultural Science and Technology Innovation Program grant to X.F.D, and the Fundamental Research Funds for Central Non‐profit Scientific Institution (Y2016CG11, S2016JC05, S2016CG01). Dan Wang, Li Tian, Dan‐Dan Zhang and Jian Song contributed equally to this work. |
ORCID | 0000-0002-2075-1835 0000-0002-8040-099X |
OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7170778/ |
PMID | 32314529 |
PQID | 2392117845 |
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PublicationCentury | 2000 |
PublicationDate | May 2020 |
PublicationDateYYYYMMDD | 2020-05-01 |
PublicationDate_xml | – month: 05 year: 2020 text: May 2020 |
PublicationDecade | 2020 |
PublicationPlace | England |
PublicationPlace_xml | – name: England – name: Oxford – name: Hoboken |
PublicationTitle | Molecular plant pathology |
PublicationTitleAlternate | Mol Plant Pathol |
PublicationYear | 2020 |
Publisher | John Wiley & Sons, Inc John Wiley and Sons Inc |
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Snippet | Secreted small cysteine‐rich proteins (SCPs) play a critical role in modulating host immunity in plant–pathogen interactions. Bioinformatic analyses showed... Secreted small cysteine-rich proteins (SCPs) play a critical role in modulating host immunity in plant-pathogen interactions. Bioinformatic analyses showed... Abstract Secreted small cysteine‐rich proteins (SCPs) play a critical role in modulating host immunity in plant–pathogen interactions. Bioinformatic analyses... |
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SubjectTerms | Amino acids Analysis Apoptosis Ascomycota - pathogenicity Cell death Chromosomes Cysteine Cystine disulphide bonds effector Gene expression Gene Expression Regulation, Plant Genes Genetic engineering Genomes Host plants Host-Pathogen Interactions - genetics Host-Pathogen Interactions - physiology Immunity Infections Original Pathogen-Associated Molecular Pattern Molecules - metabolism Pathogens pathogen‐associated molecular pattern (PAMPs) Peptides Plant Diseases - genetics Plant Diseases - microbiology Proteins Reactive oxygen species Site-directed mutagenesis small cysteine‐rich proteins (SCPs) Verticillium dahliae Virulence Virulence (Microbiology) |
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Title | Functional analyses of small secreted cysteine‐rich proteins identified candidate effectors in Verticillium dahliae |
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