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...

Full description

Saved in:
Bibliographic Details
Published inMolecular plant pathology Vol. 21; no. 5; pp. 667 - 685
Main Authors Wang, Dan, Tian, Li, Zhang, Dan‐Dan, Song, Jian, Song, Shuang‐Shuang, Yin, Chun‐Mei, Zhou, Lei, Liu, Yan, Wang, Bao‐Li, Kong, Zhi‐Qiang, Klosterman, Steven J., Li, Jun‐Jiao, Wang, Jie, Li, Ting‐Gang, Adamu, Sabiu, Subbarao, Krishna V., Chen, Jie‐Yin, Dai, Xiao‐Feng
Format Journal Article
LanguageEnglish
Published England John Wiley & Sons, Inc 01.05.2020
John Wiley and Sons Inc
Subjects
Online AccessGet full text

Cover

Loading…
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.
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
BookMark eNp1Uc1u1DAQtlAR_YEDL4AsceKw29hO4uSCVFWUIhXRQ8XVmtjjrqskXuykaG88As_IkzDblAoO2JI9nvnm88x8x-xgjCMy9loUa0HrdNhu10K2UjxjR0LV5UrpQh2QXZJdaykP2XHOd0UhdCurF-xQSSXKSrZHbL6YRzuFOELPgY5dxsyj53mAvucZbcIJHbe7PGEY8dePnynYDd-muH9nHhyOU_Bhj4HRBQcTcvQe7RQThUf-FdMUbOj7MA_cwaYPgC_Zcw99xleP9wm7ufhwc365uvry8dP52dXKlo0Uq7auwDeyg6pQ6AV0DnRblW0r0ekWGgBPbQiAktzC2a7SBfrKubpQte7UCXu_0G7nbkBnqdQEvdmmMEDamQjB_BsZw8bcxnujhS60bojg7SNBit9mzJO5i3OiMWUjFc1b6KasCLVeULfQowmjj0RmaTscgiWpfCD_mVZSKFk1khLeLQk2xZwT-qeSRGH2ihpS1DwoStg3f_fwhPwjIQFOF8B3-mX3fybz-fp6ofwNSZiw1w
CitedBy_id crossref_primary_10_3390_biom13010157
crossref_primary_10_1128_spectrum_01452_23
crossref_primary_10_3389_ffunb_2021_718557
crossref_primary_10_3389_fmicb_2022_852571
crossref_primary_10_1016_j_ygeno_2021_09_015
crossref_primary_10_1093_plphys_kiab274
crossref_primary_10_1038_s41598_022_21858_1
crossref_primary_10_3390_jof8010059
crossref_primary_10_3390_jof9070740
crossref_primary_10_1111_mpp_13213
crossref_primary_10_1111_ppa_13660
crossref_primary_10_3390_jof7121027
crossref_primary_10_1016_S2095_3119_20_63353_6
crossref_primary_10_1111_mpp_13237
crossref_primary_10_1186_s42397_021_00111_6
crossref_primary_10_1186_s42483_023_00187_9
crossref_primary_10_1111_jipb_13031
crossref_primary_10_3389_fmicb_2023_1177078
crossref_primary_10_1111_pce_14893
crossref_primary_10_3389_fmicb_2023_1130468
crossref_primary_10_1016_j_micpath_2023_106276
crossref_primary_10_3390_ijms24119403
crossref_primary_10_1111_brv_12863
crossref_primary_10_1111_mpp_13041
crossref_primary_10_1111_nph_19755
crossref_primary_10_3390_ijms23031614
crossref_primary_10_3390_plants13111523
crossref_primary_10_1186_s12915_022_01254_x
crossref_primary_10_1128_aem_00604_21
crossref_primary_10_3390_ijms232113567
crossref_primary_10_3390_pathogens12040561
crossref_primary_10_1128_mBio_01620_21
crossref_primary_10_1186_s42483_022_00135_z
crossref_primary_10_3389_fmicb_2022_941991
crossref_primary_10_1094_MPMI_09_22_0187_R
crossref_primary_10_1111_tpj_15945
crossref_primary_10_1039_D2CB00039C
crossref_primary_10_3390_ijms232314752
crossref_primary_10_1111_jipb_13162
crossref_primary_10_3390_jof8080852
crossref_primary_10_1039_D2CB00155A
crossref_primary_10_3390_jof9050574
crossref_primary_10_3390_jof7090701
crossref_primary_10_1128_msystems_01208_23
crossref_primary_10_3390_jof10040299
crossref_primary_10_1111_jph_13247
crossref_primary_10_1186_s12864_023_09811_6
Cites_doi 10.1016/j.pbi.2009.06.003
10.1016/j.cell.2006.02.008
10.1038/nmeth.1701
10.1038/ncomms5686
10.1002/j.1460-2075.1995.tb00090.x
10.1016/j.coi.2007.11.003
10.1101/gr.152660.112
10.1016/j.fbr.2016.04.001
10.1146/annurev.arplant.57.032905.105346
10.1094/MPMI-12-17-0289-R
10.1074/jbc.M212196200
10.1371/journal.ppat.1005435
10.1111/mpp.12303
10.1073/pnas.1119623109
10.1094/MPMI-12-11-0319
10.1093/nar/gkm259
10.1021/bi0023089
10.1105/tpc.113.117010
10.7554/eLife.34902
10.1038/nrmicro3119
10.1371/journal.pone.0029847
10.1016/j.jgg.2013.04.006
10.1111/j.1365-313X.2006.02837.x
10.3390/ijms161023970
10.1016/j.bbapap.2015.02.004
10.1007/PL00000835
10.1006/jmbi.2000.4315
10.1016/j.pbi.2012.05.006
10.1111/nph.13794
10.1016/S0378-1119(97)00330-2
10.1094/MPMI-4-052
10.1038/nrm954
10.1371/journal.ppat.1000290
10.1093/nar/gkm256
10.1105/tpc.109.070664
10.1038/nature05286
10.1094/MPMI-09-12-0222-R
10.1111/1462-2920.13610
10.1080/00288233.1968.10422412
10.1111/j.1364-3703.2006.00323.x
10.1093/nar/25.17.3389
10.1046/j.1365-2958.2002.03060.x
10.1111/nph.14861
10.1371/journal.ppat.1005827
10.1016/j.femsle.2005.09.014
10.1073/pnas.1220015110
10.1146/annurev-phyto-080508-081748
10.1146/annurev-phyto-080417-050141
10.1105/tpc.16.00557
10.1111/j.1364-3703.2010.00647.x
10.1146/annurev-phyto-080614-120224
10.1111/mpp.12569
10.1094/PHYTO-09-15-0215-R
10.1371/journal.ppat.1000061
10.3389/fpls.2016.00186
10.1371/journal.pone.0027217
10.1105/tpc.15.00390
10.1038/nrg2812
10.1006/meth.2001.1262
10.1146/annurev.phyto.112408.132637
10.1094/MPMI-06-17-0136-R
10.1094/PHYTO-11-13-0315-IA
10.1111/mpp.12520
10.1371/journal.ppat.1002467
10.1146/annurev.phyto.44.070505.143436
10.1146/annurev-phyto-080615-100204
10.1371/journal.ppat.1002137
10.1111/nph.14537
10.1093/nar/29.1.37
10.1111/j.1365-2958.2008.06270.x
10.1111/1462-2920.13695
10.1016/j.gene.2013.06.089
10.1046/j.1365-313X.2002.01297.x
10.3389/fmicb.2016.01709
10.1146/annurev-phyto-080614-120114
ContentType Journal Article
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.
Copyright_xml – notice: 2020 The Authors. published by British Society for Plant Pathology and John Wiley & Sons Ltd
– notice: 2020 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd.
– notice: COPYRIGHT 2020 John Wiley & Sons, Inc.
– notice: 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.
DBID 24P
WIN
CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
3V.
7QL
7QO
7T7
7U9
7X2
8FD
8FE
8FH
8FK
ABUWG
AFKRA
ATCPS
AZQEC
BBNVY
BENPR
BHPHI
C1K
CCPQU
DWQXO
FR3
GNUQQ
H94
HCIFZ
LK8
M0K
M7N
M7P
P64
PIMPY
PQEST
PQQKQ
PQUKI
PRINS
5PM
DOI 10.1111/mpp.12921
DatabaseName Wiley Open Access Journals
Wiley-Blackwell Open Access Backfiles
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
CrossRef
ProQuest Central (Corporate)
Bacteriology Abstracts (Microbiology B)
Biotechnology Research Abstracts
Industrial and Applied Microbiology Abstracts (Microbiology A)
Virology and AIDS Abstracts
Agricultural Science Collection
Technology Research Database
ProQuest SciTech Collection
ProQuest Natural Science Collection
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest Central
Agricultural & Environmental Science Collection
ProQuest Central Essentials
Biological Science Collection
AUTh Library subscriptions: ProQuest Central
ProQuest Natural Science Collection
Environmental Sciences and Pollution Management
ProQuest One Community College
ProQuest Central Korea
Engineering Research Database
ProQuest Central Student
AIDS and Cancer Research Abstracts
SciTech Premium Collection (Proquest) (PQ_SDU_P3)
ProQuest Biological Science Collection
Agriculture Science Database
Algology Mycology and Protozoology Abstracts (Microbiology C)
Biological Science Database
Biotechnology and BioEngineering Abstracts
Publicly Available Content Database
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
PubMed Central (Full Participant titles)
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
CrossRef
Agricultural Science Database
Publicly Available Content Database
ProQuest Central Student
Technology Research Database
ProQuest Central Essentials
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest Natural Science Collection
ProQuest Central China
Environmental Sciences and Pollution Management
ProQuest Central
Biotechnology Research Abstracts
Natural Science Collection
ProQuest Central Korea
Bacteriology Abstracts (Microbiology B)
Algology Mycology and Protozoology Abstracts (Microbiology C)
Agricultural & Environmental Science Collection
Biological Science Collection
AIDS and Cancer Research Abstracts
Industrial and Applied Microbiology Abstracts (Microbiology A)
Virology and AIDS Abstracts
ProQuest Biological Science Collection
ProQuest One Academic Eastern Edition
Agricultural Science Collection
Biological Science Database
ProQuest SciTech Collection
Biotechnology and BioEngineering Abstracts
ProQuest One Academic UKI Edition
Engineering Research Database
ProQuest One Academic
ProQuest Central (Alumni)
DatabaseTitleList CrossRef
Agricultural Science Database
MEDLINE



Database_xml – sequence: 1
  dbid: 24P
  name: Wiley Open Access Journals
  url: https://authorservices.wiley.com/open-science/open-access/browse-journals.html
  sourceTypes: Publisher
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
– sequence: 4
  dbid: BENPR
  name: AUTh Library subscriptions: ProQuest Central
  url: https://www.proquest.com/central
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Agriculture
DocumentTitleAlternate WANG et al
EISSN 1364-3703
EndPage 685
ExternalDocumentID A732132582
10_1111_mpp_12921
32314529
MPP12921
Genre article
Research Support, Non-U.S. Gov't
Journal Article
GrantInformation_xml – fundername: National Key Research and Development Program of China
  funderid: 2017YFD0201900; 2017YFD0200601
– fundername: Young Elite Scientists Sponsorship Program
  funderid: 2016QNRC001
– fundername: Agricultural Science and Technology Innovation Program
– fundername: Special Public Welfare Industry Research on Agriculture
  funderid: 201503109
– fundername: National Natural Science Foundation of China
  funderid: 31671986; 31471759; 31501588; 31772245; 31870138
– fundername: Fundamental Research Funds for Central Non‐profit Scientific Institution
  funderid: Y2016CG11; S2016JC05; S2016CG01
– fundername: ;
  grantid: 31671986; 31471759; 31501588; 31772245; 31870138
– fundername: National Key Research and Development Program of China
  grantid: 2017YFD0201900; 2017YFD0200601
– fundername: Fundamental Research Funds for Central Non‐profit Scientific Institution
  grantid: Y2016CG11; S2016JC05; S2016CG01
– fundername: Young Elite Scientists Sponsorship Program
  grantid: 2016QNRC001
– fundername: Special Public Welfare Industry Research on Agriculture
  grantid: 201503109
GroupedDBID ---
.3N
.GA
.Y3
05W
0R~
10A
123
1OC
24P
29M
31~
33P
3SF
4.4
50Y
50Z
51W
51X
52M
52N
52O
52P
52S
52T
52U
52W
52X
53G
5HH
5LA
5VS
66C
702
7PT
7X2
8-0
8-1
8-3
8-4
8-5
8UM
930
A03
AAESR
AAEVG
AAHBH
AAHHS
AAONW
AAZKR
ABCQN
ABDBF
ABEML
ABPVW
ACBWZ
ACCFJ
ACGFO
ACGFS
ACIWK
ACPRK
ACSCC
ACXQS
ADBBV
ADEOM
ADIZJ
ADKYN
ADZMN
AEEZP
AEGXH
AEIMD
AENEX
AEQDE
AEUQT
AFBPY
AFEBI
AFKRA
AFPWT
AFRAH
AFZJQ
AIWBW
AJBDE
AJXKR
ALAGY
ALMA_UNASSIGNED_HOLDINGS
ALUQN
AMBMR
ASPBG
ATCPS
ATUGU
AUFTA
AVUZU
AVWKF
AZBYB
AZFZN
AZVAB
BAFTC
BBNVY
BCNDV
BDRZF
BENPR
BFHJK
BHBCM
BHPHI
BMNLL
BMXJE
BNHUX
BROTX
BRXPI
BY8
CAG
CCPQU
COF
CS3
D-E
D-F
DCZOG
DPXWK
DR2
DU5
EAD
EAP
EBD
EBS
ECGQY
EDH
EJD
EMK
EMOBN
EST
ESX
F00
F01
F04
F5P
FEDTE
FRP
G-S
G.N
GODZA
GROUPED_DOAJ
H.T
H.X
HCIFZ
HF~
HVGLF
HYE
HZI
HZ~
IAO
IEP
IGS
IHE
IX1
J0M
K48
LC2
LC3
LH4
LITHE
LOXES
LP6
LP7
LUTES
LW6
M0K
M7P
MK4
MRFUL
MRSTM
MSFUL
MSSTM
N04
N05
N9A
NF~
O66
O9-
OIG
OK1
P2P
P2W
P2X
P4D
PIMPY
Q.N
Q11
QB0
R.K
ROL
RPM
RX1
SUPJJ
SV3
TUS
UB1
V8K
W8V
W99
WBKPD
WIH
WIK
WIN
WNSPC
WOHZO
WQJ
WRC
WYISQ
XG1
~IA
~KM
~WT
CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
ACXME
ADAWD
AFVGU
3V.
7QL
7QO
7T7
7U9
8FD
8FE
8FH
8FK
ABUWG
AZQEC
C1K
DWQXO
FR3
GNUQQ
H94
LK8
M7N
P64
PQEST
PQQKQ
PQUKI
PRINS
5PM
ITC
ID FETCH-LOGICAL-c4821-965af82ba503ef1abda7954992ed79a8aaf1451aa47951dcb570ef5dd60367b3
IEDL.DBID RPM
ISSN 1464-6722
IngestDate Tue Sep 17 21:26:16 EDT 2024
Fri Sep 13 02:35:03 EDT 2024
Fri Feb 02 04:16:57 EST 2024
Fri Aug 23 03:25:52 EDT 2024
Fri Sep 17 21:06:38 EDT 2021
Sat Aug 24 01:07:16 EDT 2024
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 5
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.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c4821-965af82ba503ef1abda7954992ed79a8aaf1451aa47951dcb570ef5dd60367b3
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
PQPubID 1006541
PageCount 19
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_7170778
proquest_journals_2392117845
gale_infotracacademiconefile_A732132582
crossref_primary_10_1111_mpp_12921
pubmed_primary_32314529
wiley_primary_10_1111_mpp_12921_MPP12921
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
Publisher_xml – name: John Wiley & Sons, Inc
– name: John Wiley and Sons Inc
References 2010; 11
2009; 47
2013; 26
2013; 25
2005; 253
2013; 529
2013; 23
1997; 198
2016; 30
2016; 106
2011; 12
2008; 4
2012; 15
2001; 305
2003; 278
2001; 40
2007; 35
2016a; 7
2018; 7
2009; 12
2010; 22
2014; 5
2013; 11
2018; 217
2008; 69
1999; 11
2013; 110
2008; 20
2012; 25
2018; 31
2001; 58
1968; 11
2006; 444
2006; 124
1991; 4
2015; 16
2016b; 17
2002; 30
2009; 60
1995; 14
2015; 53
2013; 40
1997; 25
2002; 453
2006; 7
2016; 54
2002; 3
2015; 1854
2017; 29
2001; 29
2011; 6
2001; 25
2011; 8
2011; 7
2017; 215
2012; 109
2016; 12
2018; 19
2016; 7
2015; 27
2006; 44
2006; 47
2016; 210
2017; 19
2017; 18
2009; 5
2018; 56
2012; 7
2014; 104
2012; 8
e_1_2_8_28_1
e_1_2_8_24_1
e_1_2_8_47_1
e_1_2_8_26_1
e_1_2_8_49_1
e_1_2_8_68_1
e_1_2_8_3_1
e_1_2_8_5_1
e_1_2_8_7_1
e_1_2_8_9_1
e_1_2_8_20_1
e_1_2_8_43_1
e_1_2_8_66_1
e_1_2_8_22_1
e_1_2_8_45_1
e_1_2_8_64_1
e_1_2_8_62_1
e_1_2_8_41_1
e_1_2_8_60_1
e_1_2_8_17_1
e_1_2_8_19_1
e_1_2_8_13_1
e_1_2_8_36_1
e_1_2_8_59_1
e_1_2_8_15_1
e_1_2_8_38_1
e_1_2_8_57_1
e_1_2_8_70_1
e_1_2_8_32_1
e_1_2_8_55_1
e_1_2_8_11_1
e_1_2_8_34_1
e_1_2_8_53_1
e_1_2_8_76_1
e_1_2_8_51_1
e_1_2_8_74_1
e_1_2_8_30_1
e_1_2_8_72_1
e_1_2_8_25_1
e_1_2_8_46_1
e_1_2_8_27_1
e_1_2_8_48_1
e_1_2_8_69_1
e_1_2_8_2_1
e_1_2_8_4_1
e_1_2_8_6_1
e_1_2_8_8_1
e_1_2_8_21_1
e_1_2_8_42_1
e_1_2_8_67_1
e_1_2_8_23_1
e_1_2_8_44_1
e_1_2_8_65_1
e_1_2_8_63_1
e_1_2_8_40_1
e_1_2_8_61_1
e_1_2_8_18_1
e_1_2_8_39_1
e_1_2_8_14_1
e_1_2_8_35_1
e_1_2_8_16_1
e_1_2_8_37_1
e_1_2_8_58_1
Jones L. (e_1_2_8_29_1) 1999; 11
e_1_2_8_10_1
e_1_2_8_31_1
e_1_2_8_56_1
e_1_2_8_77_1
e_1_2_8_12_1
e_1_2_8_33_1
e_1_2_8_54_1
e_1_2_8_75_1
e_1_2_8_52_1
e_1_2_8_73_1
e_1_2_8_50_1
e_1_2_8_71_1
References_xml – volume: 47
  start-page: 233
  year: 2009
  end-page: 263
  article-title: Fungal effector proteins
  publication-title: Annual Review of Phytopathology
– volume: 56
  start-page: 405
  year: 2018
  end-page: 426
  article-title: The rise and rise of : a plant for all reasons
  publication-title: Annual Review of Phytopathology
– volume: 7
  start-page: 71
  year: 2006
  end-page: 86
  article-title: Physiology and molecular aspects of Verticillium wilt diseases caused by and
  publication-title: Molecular Plant Pathology
– volume: 7
  start-page: 186
  year: 2016
  article-title: Kingdom‐wide analysis of fungal small secreted proteins (SSPs) reveals their potential role in host association
  publication-title: Frontiers in Plant Science
– volume: 11
  start-page: 800
  year: 2013
  end-page: 814
  article-title: Filamentous plant pathogen effectors in action
  publication-title: Nature Reviews Microbiology
– volume: 12
  start-page: 414
  year: 2009
  end-page: 420
  article-title: Early molecular events in PAMP‐triggered immunity
  publication-title: Current Opinion in Plant Biology
– volume: 6
  year: 2011
  article-title: Rust secreted protein ps87 is conserved in diverse fungal pathogens and contains a RXLR‐like motif sufficient for translocation into plant cells
  publication-title: PLoS ONE
– volume: 444
  start-page: 323
  year: 2006
  end-page: 329
  article-title: The plant immune system
  publication-title: Nature
– volume: 19
  start-page: 1914
  year: 2017
  end-page: 1932
  article-title: manipulates plant immunity by glycoside hydrolase 12 proteins in conjunction with carbohydrate‐binding module 1
  publication-title: Environmental Microbiology
– volume: 12
  year: 2016
  article-title: A small cysteine‐rich protein from the asian soybean rust fungus, , suppresses plant immunity
  publication-title: PLoS Pathogens
– volume: 17
  start-page: 577
  year: 2016b
  end-page: 587
  article-title: SCR96, a small cysteine‐rich secretory protein of , can trigger cell death in the Solanaceae and is important for pathogenicity and oxidative stress tolerance
  publication-title: Molecular Plant Pathology
– volume: 11
  start-page: 797
  year: 1968
  end-page: 802
  article-title: Verticillium wilt of tobacco
  publication-title: New Zealand Journal of Agricultural Research
– volume: 29
  start-page: 37
  year: 2001
  end-page: 40
  article-title: The InterPro database, an integrated documentation resource for protein families, domains and functional sites
  publication-title: Nucleic Acids Research
– volume: 7
  year: 2011
  article-title: Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens
  publication-title: PLoS Pathogens
– volume: 18
  start-page: 596
  year: 2017
  end-page: 608
  article-title: LysM effectors differentially contribute to virulence on plant hosts
  publication-title: Molecular Plant Pathology
– volume: 30
  start-page: 415
  year: 2002
  end-page: 429
  article-title: Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for ‐mediated resistance to tobacco mosaic virus
  publication-title: The Plant Journal
– volume: 19
  start-page: 841
  year: 2018
  end-page: 857
  article-title: transcription factor VdFTF1 regulates the expression of multiple secreted virulence factors and is required for full virulence in cotton
  publication-title: Molecular Plant Pathology
– volume: 305
  start-page: 567
  year: 2001
  end-page: 580
  article-title: Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes
  publication-title: Journal of Molecular Biology
– volume: 60
  start-page: 379
  year: 2009
  end-page: 406
  article-title: A renaissance of elicitors: perception of microbe‐associated molecular patterns and danger signals by pattern‐recognition receptors
  publication-title: Annual Review of Plant Biology
– volume: 69
  start-page: 119
  year: 2008
  end-page: 136
  article-title: The novel lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species
  publication-title: Molecular Microbiology
– volume: 210
  start-page: 743
  year: 2016
  end-page: 761
  article-title: EffectorP: predicting fungal effector proteins from secretomes using machine learning
  publication-title: New Phytologist
– volume: 8
  start-page: 785
  year: 2011
  end-page: 786
  article-title: SignalP 4.0: discriminating signal peptides from transmembrane regions
  publication-title: Nature Methods
– volume: 40
  start-page: 3458
  year: 2001
  end-page: 3466
  article-title: Disulfide bond structure of the AVR9 elicitor of the fungal tomato pathogen : evidence for a cystine knot
  publication-title: Biochemistry
– volume: 7
  year: 2012
  article-title: Using hierarchical clustering of secreted protein families to classify and rank candidate effectors of rust fungi
  publication-title: PLoS ONE
– volume: 31
  start-page: 260
  year: 2018
  end-page: 273
  article-title: A extracellular cutinase modulates plant immune responses
  publication-title: Molecular Plant‐Microbe Interactions
– volume: 110
  start-page: 10010
  year: 2013
  end-page: 10015
  article-title: Receptor‐like kinase SOBIR1/EVR interacts with receptor‐like proteins in plant immunity against fungal infection
  publication-title: Proceedings of the National Academy of Sciences of the United States of America
– volume: 215
  start-page: 368
  year: 2017
  end-page: 381
  article-title: The ‐specific protein VdSCP7 localizes to the plant nucleus and modulates immunity to fungal infections
  publication-title: New Phytologist
– volume: 529
  start-page: 307
  year: 2013
  end-page: 316
  article-title: Molecular characterization and functional analysis of a specific secreted protein from highly virulent defoliating
  publication-title: Gene
– volume: 25
  start-page: 402
  year: 2001
  end-page: 408
  article-title: Analysis of relative gene expression data using real‐time quantitative PCR and the 2 method
  publication-title: Methods
– volume: 35
  start-page: W429
  year: 2007
  end-page: 432
  article-title: Advantages of combined transmembrane topology and signal peptide prediction‐the Phobius web server
  publication-title: Nucleic Acids Research
– volume: 124
  start-page: 803
  year: 2006
  end-page: 814
  article-title: Host–microbe interactions: shaping the evolution of the plant immune response
  publication-title: Cell
– volume: 4
  year: 2008
  article-title: Suppression of plant resistance gene‐based immunity by a fungal effector
  publication-title: PLoS Pathogens
– volume: 25
  start-page: 4227
  year: 2013
  end-page: 4241
  article-title: Arabidopsis receptor‐like protein30 and receptor‐like kinase suppressor of BIR1‐1/EVERSHED mediate innate immunity to necrotrophic fungi
  publication-title: The Plant Cell
– volume: 217
  start-page: 756
  year: 2018
  end-page: 770
  article-title: Comparative genomics reveals cotton‐specific virulence factors in flexible genomic regions in and evidence of horizontal gene transfer from
  publication-title: New Phytologist
– volume: 29
  start-page: 2871
  year: 2017
  end-page: 2881
  article-title: Host‐mediated S‐nitrosylation disarms the bacterial effector HopAI1 to reestablish immunity
  publication-title: The Plant Cell
– volume: 12
  year: 2016
  article-title: A small secreted virulence‐related protein is essential for the necrotrophic interactions of with its host plants
  publication-title: PLoS Pathogens
– volume: 44
  start-page: 41
  year: 2006
  end-page: 60
  article-title: A catalogue of the effector secretome of plant pathogenic oomycetes
  publication-title: Annual Review of Phytopathology
– volume: 106
  start-page: 166
  year: 2016
  end-page: 176
  article-title: Genome‐wide analysis of small secreted cysteine‐rich proteins identifies candidate effector proteins potentially involved in ‐wheat interactions
  publication-title: Phytopathology
– volume: 198
  start-page: 289
  year: 1997
  end-page: 296
  article-title: A genetic selection for isolating cDNAs encoding secreted proteins
  publication-title: Gene
– volume: 22
  start-page: 260
  year: 2010
  end-page: 272
  article-title: Tomato 14‐3‐3 protein 7 positively regulates immunity‐associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKKα
  publication-title: The Plant Cell
– volume: 25
  start-page: 964
  year: 2012
  end-page: 975
  article-title: Molecular characterization and functional analysis of a necrosis‐ and ethylene‐inducing, protein‐encoding gene family from
  publication-title: Molecular Plant‐Microbe Interactions
– volume: 3
  start-page: 836
  year: 2002
  end-page: 847
  article-title: Formation and transfer of disulphide bonds in living cells
  publication-title: Nature Reviews Molecular Cell Biology
– volume: 53
  start-page: 541
  year: 2015
  end-page: 563
  article-title: Understanding plant immunity as a surveillance system to detect invasion
  publication-title: Annual Review of Phytopathology
– volume: 20
  start-page: 10
  year: 2008
  end-page: 16
  article-title: Pattern‐recognition receptors in plant innate immunity
  publication-title: Current Opinion in Immunology
– volume: 11
  start-page: 539
  year: 2010
  end-page: 548
  article-title: Plant immunity: towards an integrated view of plant–pathogen interactions
  publication-title: Nature Reviews Genetics
– volume: 15
  start-page: 349
  year: 2012
  end-page: 357
  article-title: Plant pattern recognition receptor complexes at the plasma membrane
  publication-title: Current Opinion in Plant Biology
– volume: 253
  start-page: 19
  year: 2005
  end-page: 27
  article-title: Small proteins of plant‐pathogenic fungi secreted during host colonization
  publication-title: FEMS Microbiology Letters
– volume: 47
  start-page: 851
  year: 2006
  end-page: 863
  article-title: Peroxidase‐dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance
  publication-title: The Plant Journal
– volume: 7
  start-page: 1709
  year: 2016a
  article-title: Characterization of the exoproteome involved in pathogenicity from cotton-containing medium
  publication-title: Frontiers in Microbiology
– volume: 278
  start-page: 27340
  year: 2003
  end-page: 27346
  article-title: Natural disulfide bond‐disrupted mutants of of the tomato pathogen are sensitive to proteolysis, circumvent ‐mediated resistance, but retain their chitin binding ability
  publication-title: Journal of Biological Chemistry
– volume: 453
  start-page: 875
  year: 2002
  end-page: 884
  article-title: overcomes ‐mediated resistance by producing truncated AVR2 elicitor proteins
  publication-title: Molecular Microbiology
– volume: 58
  start-page: 2043
  year: 2001
  end-page: 2052
  article-title: Transformation: a tool for studying fungal pathogens of plants
  publication-title: Cellular and Molecular Life Sciences
– volume: 11
  start-page: 2291
  year: 1999
  end-page: 2301
  article-title: RNA‐DNA interactions and DNA methylation in post‐transcriptional gene silencing
  publication-title: The Plant Cell
– volume: 30
  start-page: 62
  year: 2016
  end-page: 73
  article-title: Form and function of fungal and oomycete effectors
  publication-title: Fungal Biology Reviews
– volume: 40
  start-page: 421
  year: 2013
  end-page: 431
  article-title: Functional analysis of autophagy genes via Agrobacterium-mediated transformation in the vascular wilt fungus Verticillium dahliae
  publication-title: Journal of Genetics and Genomics
– volume: 19
  start-page: 1717
  year: 2017
  end-page: 1729
  article-title: PSTha5a23, a candidate effector from the obligate biotrophic pathogen f. sp. , is involved in plant defense suppression and rust pathogenicity
  publication-title: Environmental Microbiology
– volume: 47
  start-page: 39
  year: 2009
  end-page: 62
  article-title: Diversity, pathogenicity, and management of species
  publication-title: Annual Review of Phytopathology
– volume: 104
  start-page: 564
  year: 2014
  end-page: 574
  article-title: systematics and evolution: implications of information confusion on verticillium wilt management and potential solutions
  publication-title: Phytopathology
– volume: 27
  start-page: 2057
  year: 2015
  end-page: 2072
  article-title: A glycoside hydrolase 12 protein is a major virulence factor during soybean infection and is recognized as a PAMP
  publication-title: The Plant Cell
– volume: 35
  start-page: W585
  year: 2007
  end-page: 587
  article-title: WoLF PSORT: protein localization predictor
  publication-title: Nucleic Acids Research
– volume: 4
  start-page: 52
  year: 1991
  end-page: 59
  article-title: Cloning and characterization of cDNA of avirulence gene of the fungal pathogen , causal agent of tomato leaf mold
  publication-title: Molecular Plant‐Microbe Interactions
– volume: 53
  start-page: 181
  year: 2015
  end-page: 198
  article-title: Genomics spurs rapid advances in our understanding of the biology of vascular wilt pathogens in the genus
  publication-title: Annual Review of Phytopathology
– volume: 8
  year: 2012
  article-title: The cysteine rich necrotrophic effector SnTox1 produced by triggers susceptibility of wheat lines harboring
  publication-title: PLoS Pathogens
– volume: 5
  year: 2009
  article-title: Pep1, a secreted effector protein of , is required for successful invasion of plant cells
  publication-title: PLoS Pathogens
– volume: 26
  start-page: 278
  year: 2013
  end-page: 286
  article-title: Evidence for functional diversification within a fungal NEP1‐like protein family
  publication-title: Molecular Plant‐Microbe Interactions
– volume: 12
  start-page: 21
  year: 2011
  end-page: 30
  article-title: Affinity of Avr2 for tomato cysteine protease Rcr3 correlates with the ‐triggered ‐mediated hypersensitive response
  publication-title: Molecular Plant Pathology
– volume: 1854
  start-page: 437
  year: 2015
  end-page: 448
  article-title: Comparative analyses of secreted proteins from the phytopathogenic fungus in response to nitrogen starvation
  publication-title: Biochimica et Biophysica Acta
– volume: 31
  start-page: 651
  year: 2018
  end-page: 664
  article-title: SNARE‐encoding genes and mediate protein secretion required for full virulence in
  publication-title: Molecular Plant‐Microbe Interactions
– volume: 16
  start-page: 23970
  year: 2015
  end-page: 23993
  article-title: The role of pathogen‐secreted proteins in fungal vascular wilt diseases
  publication-title: International Journal of Molecular Sciences
– volume: 25
  start-page: 3389
  year: 1997
  end-page: 3402
  article-title: Gapped BLAST and PSI‐BLAST: a new generation of protein database search programs
  publication-title: Nucleic Acids Research
– volume: 54
  start-page: 419
  year: 2016
  end-page: 441
  article-title: Plant‐pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners
  publication-title: Annual Review of Phytopathology
– volume: 109
  start-page: 5110
  year: 2012
  end-page: 5115
  article-title: Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing
  publication-title: Proceedings of the National Academy of Sciences of the United States of America
– volume: 7
  year: 2018
  article-title: The plant‐specific transcription factors CBP60g and SARD1 are targeted by a secretory protein VdSCP41 to modulate immunity
  publication-title: eLife
– volume: 23
  start-page: 1271
  year: 2013
  end-page: 1282
  article-title: Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen
  publication-title: Genome Research
– volume: 14
  start-page: 4168
  year: 1995
  end-page: 4177
  article-title: The race‐specific elicitor, NIP1, from the barley pathogen, , determines avirulence on host plants of the resistance genotype
  publication-title: EMBO Journal
– volume: 5
  start-page: 4686
  year: 2014
  article-title: Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis
  publication-title: Nature Communications
– ident: e_1_2_8_77_1
  doi: 10.1016/j.pbi.2009.06.003
– ident: e_1_2_8_13_1
  doi: 10.1016/j.cell.2006.02.008
– ident: e_1_2_8_55_1
  doi: 10.1038/nmeth.1701
– ident: e_1_2_8_44_1
  doi: 10.1038/ncomms5686
– ident: e_1_2_8_59_1
  doi: 10.1002/j.1460-2075.1995.tb00090.x
– ident: e_1_2_8_76_1
  doi: 10.1016/j.coi.2007.11.003
– ident: e_1_2_8_31_1
  doi: 10.1101/gr.152660.112
– ident: e_1_2_8_64_1
  doi: 10.1016/j.fbr.2016.04.001
– ident: e_1_2_8_6_1
  doi: 10.1146/annurev.arplant.57.032905.105346
– ident: e_1_2_8_69_1
  doi: 10.1094/MPMI-12-17-0289-R
– ident: e_1_2_8_8_1
  doi: 10.1074/jbc.M212196200
– ident: e_1_2_8_50_1
  doi: 10.1371/journal.ppat.1005435
– ident: e_1_2_8_11_1
  doi: 10.1111/mpp.12303
– ident: e_1_2_8_30_1
  doi: 10.1073/pnas.1119623109
– ident: e_1_2_8_74_1
  doi: 10.1094/MPMI-12-11-0319
– ident: e_1_2_8_24_1
  doi: 10.1093/nar/gkm259
– ident: e_1_2_8_23_1
  doi: 10.1021/bi0023089
– ident: e_1_2_8_73_1
  doi: 10.1105/tpc.113.117010
– ident: e_1_2_8_57_1
  doi: 10.7554/eLife.34902
– ident: e_1_2_8_19_1
  doi: 10.1038/nrmicro3119
– ident: e_1_2_8_62_1
  doi: 10.1371/journal.pone.0029847
– ident: e_1_2_8_75_1
  doi: 10.1016/j.jgg.2013.04.006
– ident: e_1_2_8_5_1
  doi: 10.1111/j.1365-313X.2006.02837.x
– volume: 11
  start-page: 2291
  year: 1999
  ident: e_1_2_8_29_1
  article-title: RNA‐DNA interactions and DNA methylation in post‐transcriptional gene silencing
  publication-title: The Plant Cell
  contributor:
    fullname: Jones L.
– ident: e_1_2_8_60_1
  doi: 10.3390/ijms161023970
– ident: e_1_2_8_14_1
  doi: 10.1016/j.bbapap.2015.02.004
– ident: e_1_2_8_53_1
  doi: 10.1007/PL00000835
– ident: e_1_2_8_40_1
  doi: 10.1006/jmbi.2000.4315
– ident: e_1_2_8_52_1
  doi: 10.1016/j.pbi.2012.05.006
– ident: e_1_2_8_65_1
  doi: 10.1111/nph.13794
– ident: e_1_2_8_27_1
  doi: 10.1016/S0378-1119(97)00330-2
– ident: e_1_2_8_34_1
  doi: 10.1094/MPMI-4-052
– ident: e_1_2_8_63_1
  doi: 10.1038/nrm954
– ident: e_1_2_8_17_1
  doi: 10.1371/journal.ppat.1000290
– ident: e_1_2_8_32_1
  doi: 10.1093/nar/gkm256
– ident: e_1_2_8_54_1
  doi: 10.1105/tpc.109.070664
– ident: e_1_2_8_28_1
  doi: 10.1038/nature05286
– ident: e_1_2_8_61_1
  doi: 10.1094/MPMI-09-12-0222-R
– ident: e_1_2_8_12_1
  doi: 10.1111/1462-2920.13610
– ident: e_1_2_8_70_1
  doi: 10.1080/00288233.1968.10422412
– ident: e_1_2_8_18_1
  doi: 10.1111/j.1364-3703.2006.00323.x
– ident: e_1_2_8_2_1
  doi: 10.1093/nar/25.17.3389
– ident: e_1_2_8_49_1
  doi: 10.1046/j.1365-2958.2002.03060.x
– ident: e_1_2_8_9_1
  doi: 10.1111/nph.14861
– ident: e_1_2_8_56_1
  doi: 10.1371/journal.ppat.1005827
– ident: e_1_2_8_58_1
  doi: 10.1016/j.femsle.2005.09.014
– ident: e_1_2_8_41_1
  doi: 10.1073/pnas.1220015110
– ident: e_1_2_8_38_1
  doi: 10.1146/annurev-phyto-080508-081748
– ident: e_1_2_8_4_1
  doi: 10.1146/annurev-phyto-080417-050141
– ident: e_1_2_8_42_1
  doi: 10.1105/tpc.16.00557
– ident: e_1_2_8_68_1
  doi: 10.1111/j.1364-3703.2010.00647.x
– ident: e_1_2_8_36_1
  doi: 10.1146/annurev-phyto-080614-120224
– ident: e_1_2_8_72_1
  doi: 10.1111/mpp.12569
– ident: e_1_2_8_48_1
  doi: 10.1094/PHYTO-09-15-0215-R
– ident: e_1_2_8_25_1
  doi: 10.1371/journal.ppat.1000061
– ident: e_1_2_8_35_1
  doi: 10.3389/fpls.2016.00186
– ident: e_1_2_8_20_1
  doi: 10.1371/journal.pone.0027217
– ident: e_1_2_8_51_1
  doi: 10.1105/tpc.15.00390
– ident: e_1_2_8_16_1
  doi: 10.1038/nrg2812
– ident: e_1_2_8_47_1
  doi: 10.1006/meth.2001.1262
– ident: e_1_2_8_66_1
  doi: 10.1146/annurev.phyto.112408.132637
– ident: e_1_2_8_22_1
  doi: 10.1094/MPMI-06-17-0136-R
– ident: e_1_2_8_26_1
  doi: 10.1094/PHYTO-11-13-0315-IA
– ident: e_1_2_8_39_1
  doi: 10.1111/mpp.12520
– ident: e_1_2_8_45_1
  doi: 10.1371/journal.ppat.1002467
– ident: e_1_2_8_33_1
  doi: 10.1146/annurev.phyto.44.070505.143436
– ident: e_1_2_8_67_1
  doi: 10.1146/annurev-phyto-080615-100204
– ident: e_1_2_8_37_1
  doi: 10.1371/journal.ppat.1002137
– ident: e_1_2_8_71_1
  doi: 10.1111/nph.14537
– ident: e_1_2_8_3_1
  doi: 10.1093/nar/29.1.37
– ident: e_1_2_8_7_1
  doi: 10.1111/j.1365-2958.2008.06270.x
– ident: e_1_2_8_21_1
  doi: 10.1111/1462-2920.13695
– ident: e_1_2_8_43_1
  doi: 10.1016/j.gene.2013.06.089
– ident: e_1_2_8_46_1
  doi: 10.1046/j.1365-313X.2002.01297.x
– ident: e_1_2_8_10_1
  doi: 10.3389/fmicb.2016.01709
– ident: e_1_2_8_15_1
  doi: 10.1146/annurev-phyto-080614-120114
SSID ssj0017925
Score 2.5158982
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...
SourceID pubmedcentral
proquest
gale
crossref
pubmed
wiley
SourceType Open Access Repository
Aggregation Database
Index Database
Publisher
StartPage 667
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)
SummonAdditionalLinks – databaseName: AUTh Library subscriptions: ProQuest Central
  dbid: BENPR
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Nj9MwEB0tuxc4IL4JLMhCSHAJTRwndk6ooK0qpF1VaEF7i-zY3lZK09K0d34Cv5Ffwkw-ynYluCWxE1t5tmfseX4GeCtztImZiUOtlQ1FpqPQlMpjjzeCxFUiX1JE9_wim34TX67SqyOYDnthiFY5jIntQG1XJa2Rjzga8jiWSqQjbWgVoNyOPq5_hHR-FMVZ-8M07sAJjwUFbE8-nV3Mvu4jCliptNtpJMJMct6rDBGrZ7lef0Czx-MD23R7hL5hom7TJ2-6ta1dmjyA-71DycZdC3gIR65-BPfG15teVMM9ht0EjVe35sd0K0LiGrbyrFnqqmINOY7od7KSRJ3R6fz98xe-PGethMOibtjCdpQiykO7YGiRgHVEkNUGk2v2vWNnV9Vit2RWz6uFdk_gcnJ2-Xka9scthKVQRNTIUu0VNzqNEudjbayWFATMubMy10prT8f6ai3wcWxLk8rI-dTaDK2gNMlTOK5XtXsODG9cbgyCXkbCE1_Re5MIpXOrMvxKAG-G_1ysO1GNYpiMIBhFC0YA7wiBgjoawa37_QJYBElWFWOZcJxKp4oHcDqAVPQ9sCn-tpcAnnV47ctK0KmlgHMA8gDJfQbS3D5MqRfzVnsbZ7-RlCqA9y3m_65-cT6btRcv_l-7l3CX0xS-5VCewvF2s3Ov0M_Zmtd9E_4DC_YBeA
  priority: 102
  providerName: ProQuest
– databaseName: Wiley Open Access Journals
  dbid: 24P
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV3NitswEBbL9tIeSv_r7baIUmgvLrYsWzI9hdKwFLbksC17MyNbagyOE-LNvY-wz7hP0hnJMclCoTfbkiyhT6MZSTOfGPugStSJhUljAN3EsoAkNrV2KPFGErlK4mo60b38UVz8lN-v8-sT9mUfCxP4IaYNN5IMP1-TgIMZDoR8tdl8RmVFQeQP0KzRNKSFXExHCNiKPIQWybhQQoy0QuTGMxU9Ukb3p-QDnXTfX_LQjvWKaP6EPR4tSD4LkD9lJ7Z_xh7Nfm9HFg37nO3mqK3CJh8HzzpiB752fFhB1_GBLEU0NHlNLM7YD3d_brHwknvOhrYfeNsEHyLKQ2EvtCvAg-fHeovJPf8V3LG7rt2teAPLrgX7gl3Nv119vYjH-xXiWmryzChycFoYyJPMuhRMA4pO_UphG1WCBnB0jy-AxM9pU5tcJdblTVOg2lMme8lO-3VvXzOOL7Y0BlGuE-nIQdE5k0kNZaML_EvE3u_7udoEFo1qv_pAMCoPRsQ-EgIVSRZ2cw1jgABWQRxV1UxlAtfOuRYRO9-DVI0iN1QCLb00VVrmEXsV8JrqytCKpRPmiKkjJKcMRLJ9nNK3S0-2jcvdRCkdsU8e8383v7pcLPzD2f9nfcMeClq_ewfKc3Z6s93Zt2jk3Jh3fjD_BXw1_IM
  priority: 102
  providerName: Wiley-Blackwell
Title Functional analyses of small secreted cysteine‐rich proteins identified candidate effectors in Verticillium dahliae
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fmpp.12921
https://www.ncbi.nlm.nih.gov/pubmed/32314529
https://www.proquest.com/docview/2392117845/abstract/
https://pubmed.ncbi.nlm.nih.gov/PMC7170778
Volume 21
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3Pb5swFH5qust2mPZ7bF1kTZO2CwkYg80xqxpVkxKhqpt6QzbYCxKQKDT3_Qn7G_eX7NlA1VTaZRcEGLDlz-a9Z3_-DPCJp2gTExX6UorSZ4kMfFUIgz1eMSuuEpjCzuiu1snld_btJr45gXhcC-NI-4WqZm3dzNpq47iVu6aYjzyxebY6xxAk4FzMJzDhUTSG6MPUAeYe90uKmJ9wSgc5IUvfaXa7Gdo3areHidCxsZOOR_bo4V_5nll6SJm878o6W7R8Bk8HJ5Is-sI-hxPdvoAni5_7QUhDv4TDEg1WP85HpBMe0R3ZGtI1sq5JZ51F9DVJYYWc0dH88-s3vrwhTrahajtSlT2NyD5jV77YgQHSkz-2e0xuyY-ekV3X1aEhpdzUldSv4Hp5cX1-6Q9bLPgFE5ackcTSCKpkHETahFKVktuJv5TqkqdSSGnsVr5SMrwdloWKeaBNXJYJWj6uotdw2m5b_RYIXuhUKQS6CJixHEVjVMSETEuR4Fc8-DjWc77rhTTyMQBBXHKHiwefLQK57VxYzYUc1ghgFlamKl_wiGL4HAvqwdkIUj70ui6n6OyFIRcs9uBNj9ddXiPeHvAjJO8esDrbxynY_Jze9tDcPPjiMP938fNVlrmTd_-dyXt4TG1E7yiVZ3B6uz_oD-j23KopTCjLpvDo68U6u5q6wQN7vKJ4XGerqesGfwHvgQqz
link.rule.ids 230,315,733,786,790,870,891,1382,11589,21416,27957,27958,33779,43840,46087,46329,46511,46753,50849,50958,53827,53829,74659
linkProvider National Library of Medicine
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Lj9MwEB5B9wAcEG8CC1gICS5h83Bi54QK2qrAtqpQQXuL7DimkdK0NNs7P4HfyC9hJnHLdiW45eEklr_YM-P5_BnglcjQJqY69JWSxuepCnxdSIs9XnMSVwlsQRndyTQdf-WfzpNzN-HWOlrlbkzsBmqzKmiO_CRCQx6GQvLk3fqHT7tGUXbVbaFxHY54jKHKAI7en05nX_Z5BKxK0q8v4n4qoshpCxGXZ7lev0VjF4UHFunquHzJMF0lTV52ZjtrNLoDt50byYY97nfhWtncg1vD7xsnpVHeh-0ITVY_08dUJz1StmxlWbtUdc1achfR22QFSTmjq_n75y98eME64YaqaVlleiIRlaG1LzQ1wHr6x2qDtxv2redk13W1XTKjFnWlygcwH53OP4x9t8mCX3BJ9Iw0UVZGWiVBXNpQaaMEpf6yqDQiU1IpS5v5KsXxcmgKnYigtIkxKdo-oeOHMGhWTfkYGJ6UmdYIdRFwSyxFa3XMpcqMTPEtHrzctXO-7qU08l0IgmDkHRgevCYEcupe2MyFcqsE8BMkVJUPRRxhAJ3IyIPjHUi563dt_vcv8eBRj9f-WzG6spRm9kAcILkvQErbh3eaatEpbmPMGwghPXjTYf7v6ueT2aw7ePL_2r2AG-P55Cw_-zj9_BRuRhTEdyzKYxhcbLblM_R0LvRz9zv_ASUPAKs
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Lj9MwEB7BroTggHgTWMBCSHAJm4cTOydUYKvlsVWFFrS3yI5tGilNS7O98xP4jfwSZhK3bFeCWxInseUZe2Y8nz8DvBAF2sRcx6FS0oQ8V1GoK-lwxGtO5CqRqyijezLJj7_yj2fZmcc_dR5WuZkT-4naLCpaIz9M0JDHsZA8O3QeFjF9P36z_BHSCVKUafXHaVyFfcHzDDV8_-3RZPplm1PAZmXDXiMe5iJJPM8Q4Xrmy-VrNHxJvGOdLs_RF4zUZQDlRce2t0zjW3DTu5RsNOjAbbhi2ztwY_R95Wk17F1Yj9F8Dat-TPU0JLZjC8e6uWoa1pHriJ4nq4jWGd3O3z9_4ccz1pM41G3HajOAiugd2gdDywRsgIIsVljcsm8DPrtp6vWcGTVramXvwen46PTdcegPXAgrLgmqkWfKyUSrLEqti5U2SlAasEisEYWSSjk62Fcpjo9jU-lMRNZlxuRoB4VO78Neu2jtQ2B4YwutUexVxB0hFp3TKZeqMDLHvwTwfNPP5XKg1Sg34QgKo-yFEcBLkkBJQw27uVJ-xwBWQaRV5UikCQbTmUwCONgIqfRjsCv_akwADwZ5betK0a2llHMAYkeS2xeIdXu3pK1nPfs2xr-REDKAV73M_9388mQ67S8e_b91z-AaanL5-cPk02O4nlA83wMqD2DvfLW2T9DpOddPvTb_AQr6BOg
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Functional+analyses+of+small+secreted+cysteine%E2%80%90rich+proteins+identified+candidate+effectors+in+Verticillium+dahliae&rft.jtitle=Molecular+plant+pathology&rft.au=Wang%2C+Dan&rft.au=Tian%2C+Li&rft.au=Zhang%2C+Dan%E2%80%90Dan&rft.au=Song%2C+Jian&rft.date=2020-05-01&rft.issn=1464-6722&rft.eissn=1364-3703&rft.volume=21&rft.issue=5&rft.spage=667&rft.epage=685&rft_id=info:doi/10.1111%2Fmpp.12921&rft.externalDBID=10.1111%252Fmpp.12921&rft.externalDocID=MPP12921
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1464-6722&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1464-6722&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1464-6722&client=summon