A papain-like cysteine protease-released small signal peptide confers wheat resistance to wheat yellow mosaic virus.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
27 Nov 2023
Historique:
received: 02 07 2022
accepted: 15 11 2023
medline: 29 11 2023
pubmed: 28 11 2023
entrez: 27 11 2023
Statut: epublish

Résumé

Wheat yellow mosaic virus (WYMV), a soil-borne pathogen, poses a serious threat to global wheat production. Here, we identify a WYMV resistance gene, TaRD21A, that belongs to the papain-like cysteine protease family. Through genetic manipulation of TaRD21A expression, we establish its positive role in the regulation of wheat to WYMV resistance. Furthermore, our investigation shows that the TaRD21A-mediated plant antiviral response relies on the release of a small peptide catalyzed by TaRD21A protease activity. To counteract wheat resistance, WYMV-encoded nuclear inclusion protease-a (NIa) suppress TaRD21A activity to promote virus infection. In resistant cultivars, a natural variant of TaRD21A features a glycine-to-threonine substitution and this substitution enables the phosphorylation of threonine, thereby weakening the interaction between NIa and TaRD21A, reinforcing wheat resistance against WYMV. Our study not only unveils a WYMV resistance gene but also offers insights into the intricate mechanisms underpinning resistance against WYMV.

Identifiants

pubmed: 38012219
doi: 10.1038/s41467-023-43643-y
pii: 10.1038/s41467-023-43643-y
pmc: PMC10682394
doi:

Substances chimiques

Papain EC 3.4.22.2
Protein Sorting Signals 0
Threonine 2ZD004190S

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

7773

Subventions

Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 32100126

Informations de copyright

© 2023. The Author(s).

Références

Nat Commun. 2023 Aug 4;14(1):4697
pubmed: 37542077
Mol Plant. 2020 Dec 7;13(12):1733-1751
pubmed: 32896642
Cell. 2021 Oct 14;184(21):5391-5404.e17
pubmed: 34597584
Curr Opin Plant Biol. 2019 Oct;51:22-28
pubmed: 31026543
PLoS One. 2011 Mar 15;6(3):e17573
pubmed: 21423655
Science. 2011 Dec 9;334(6061):1405-8
pubmed: 22158819
Virus Res. 2009 May;141(2):174-83
pubmed: 19159654
Trends Plant Sci. 2017 Sep;22(9):779-791
pubmed: 28779900
Plant Physiol. 2019 Jul;180(3):1375-1388
pubmed: 31019004
J Exp Bot. 2021 May 28;72(12):4472-4488
pubmed: 33681961
Nat Commun. 2022 Nov 2;13(1):6576
pubmed: 36323720
Nat Genet. 2019 Jul;51(7):1194
pubmed: 31197271
Virology. 2015 Feb;476:159-167
pubmed: 25543966
Nucleic Acids Res. 2012 Jan;40(Database issue):D400-12
pubmed: 22140110
Virology. 2021 Apr;556:101-109
pubmed: 33561697
Genome Biol. 2019 Jul 12;20(1):136
pubmed: 31300020
PLoS Pathog. 2014 Sep 04;10(9):e1004331
pubmed: 25188390
Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8807-14
pubmed: 10922039
Proc Natl Acad Sci U S A. 2023 Mar 14;120(11):e2214968120
pubmed: 36897977
BMC Plant Biol. 2019 Apr 23;19(1):153
pubmed: 31014249
Plant Sci. 2014 Nov;228:135-49
pubmed: 25438794
Nat Plants. 2018 Mar;4(3):172-180
pubmed: 29483684
Theor Appl Genet. 2020 May;133(5):1623-1640
pubmed: 32008056
Virus Genes. 2019 Apr;55(2):209-217
pubmed: 30565034
Semin Thromb Hemost. 2006 Apr;32 Suppl 1:39-48
pubmed: 16673265
Mol Plant Pathol. 2021 Apr;22(4):456-464
pubmed: 33629491
Theor Appl Genet. 2012 Jan;124(1):177-88
pubmed: 21959905
New Phytol. 2020 Apr;226(1):205-220
pubmed: 31815302
Plant Biotechnol J. 2019 Nov;17(11):2106-2122
pubmed: 30963678
Proc Natl Acad Sci U S A. 2011 Dec 20;108(51):20832-7
pubmed: 22143776
Plant Biotechnol J. 2017 Aug;15(8):953-969
pubmed: 28055148
Plant Signal Behav. 2012 Aug;7(8):983-9
pubmed: 22827939
New Phytol. 2016 Dec;212(4):902-907
pubmed: 27488095
PLoS Genet. 2012;8(7):e1002813
pubmed: 22829777
J Plant Res. 2018 Sep;131(5):827-837
pubmed: 29730747
Mol Plant. 2021 Nov 1;14(11):1881-1900
pubmed: 34303025
PLoS One. 2012;7(1):e29317
pubmed: 22238602
PLoS Pathog. 2013 Feb;9(2):e1003177
pubmed: 23459172
New Phytol. 2010 Jan;185(1):258-74
pubmed: 19825016
Plant Dis. 2000 Jun;84(6):627-630
pubmed: 30841101
Bioinformatics. 2012 Sep 15;28(18):2397-9
pubmed: 22796960
Plant Cell. 2008 Apr;20(4):1169-83
pubmed: 18451324
Plant Biotechnol J. 2014 May;12(4):447-56
pubmed: 24373454
Front Plant Sci. 2014 Jun 03;5:249
pubmed: 24917874
Annu Rev Phytopathol. 2021 Aug 25;59:1-29
pubmed: 33891829
Biology (Basel). 2019 Oct 23;8(4):
pubmed: 31652738
Cell. 2017 Jun 29;170(1):114-126.e15
pubmed: 28666113
Phytochemistry. 2011 Jul;72(10):975-96
pubmed: 21353264
Nat Genet. 2019 May;51(5):905-911
pubmed: 31043760
Methods. 2001 Dec;25(4):402-8
pubmed: 11846609
Am J Hum Genet. 2007 Sep;81(3):559-75
pubmed: 17701901
Front Plant Sci. 2015 Aug 03;6:584
pubmed: 26284100
Mol Plant Microbe Interact. 2013 Sep;26(9):1004-15
pubmed: 23697374
Plant Cell. 2022 Jul 30;34(8):3110-3127
pubmed: 35567529
Plant Physiol. 2010 Dec;154(4):1794-804
pubmed: 20940351
Mol Biol Evol. 2016 Jul;33(7):1870-4
pubmed: 27004904
Biochem Biophys Res Commun. 2015 May 8;460(3):525-9
pubmed: 25797621
Proc Natl Acad Sci U S A. 2012 Jun 19;109(25):10119-24
pubmed: 22675118
Nat Commun. 2022 Feb 7;13(1):716
pubmed: 35132090
Plant Dis. 2018 May;102(5):948-954
pubmed: 30673393
Science. 2014 Jul 18;345(6194):1250091
pubmed: 25035498
Arch Virol. 1998;143(4):631-43
pubmed: 9638137
Nat Biotechnol. 2013 Aug;31(8):686-8
pubmed: 23929338
PLoS Pathog. 2019 Apr 18;15(4):e1007728
pubmed: 30998777
Plant Biotechnol J. 2016 Oct;14(10):1941-55
pubmed: 26990124

Auteurs

Peng Liu (P)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.

Chaonan Shi (C)

National Key Laboratory of Wheat and Maize Crop Science/CIMMYT-China Wheat and Maize Joint Research Center/Agronomy College, Henan Agricultural University, Zhengzhou, 450002, China.

Shuang Liu (S)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.

Jiajia Lei (J)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.

Qisen Lu (Q)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.

Haichao Hu (H)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.

Yan Ren (Y)

National Key Laboratory of Wheat and Maize Crop Science/CIMMYT-China Wheat and Maize Joint Research Center/Agronomy College, Henan Agricultural University, Zhengzhou, 450002, China.

Ning Zhang (N)

National Key Laboratory of Wheat and Maize Crop Science/CIMMYT-China Wheat and Maize Joint Research Center/Agronomy College, Henan Agricultural University, Zhengzhou, 450002, China.

Congwei Sun (C)

National Key Laboratory of Wheat and Maize Crop Science/CIMMYT-China Wheat and Maize Joint Research Center/Agronomy College, Henan Agricultural University, Zhengzhou, 450002, China.

Lu Chen (L)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.

Yaoyao Jiang (Y)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.

Lixiao Feng (L)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.

Tianye Zhang (T)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.

Kaili Zhong (K)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.

Jiaqian Liu (J)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.

Juan Zhang (J)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.

Zhuo Zhang (Z)

Hunan Plant Protection Institute, Hunan Academy of Agricultural Sciences, Changsha, 410152, China.

Bingjian Sun (B)

National Key Laboratory of Wheat and Maize Crop Science/CIMMYT-China Wheat and Maize Joint Research Center/Agronomy College, Henan Agricultural University, Zhengzhou, 450002, China.

Jianping Chen (J)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China. jpchen2001@126.com.

Yimiao Tang (Y)

Institute of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China. tangyimiao@126.com.

Feng Chen (F)

National Key Laboratory of Wheat and Maize Crop Science/CIMMYT-China Wheat and Maize Joint Research Center/Agronomy College, Henan Agricultural University, Zhengzhou, 450002, China. chf0088@163.com.

Jian Yang (J)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Rural Affairs and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China. nather2008@163.com.

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