TOM1 family conservation within the plant kingdom for tobacco mosaic virus accumulation.


Journal

Molecular plant pathology
ISSN: 1364-3703
Titre abrégé: Mol Plant Pathol
Pays: England
ID NLM: 100954969

Informations de publication

Date de publication:
11 2023
Historique:
revised: 03 06 2023
received: 17 03 2023
accepted: 26 06 2023
medline: 23 10 2023
pubmed: 14 7 2023
entrez: 14 7 2023
Statut: ppublish

Résumé

The susceptibility factor TOBAMOVIRUS MULTIPLICATION 1 (TOM1) is required for efficient multiplication of tobacco mosaic virus (TMV). Although some phylogenetic and functional analyses of the TOM1 family members have been conducted, a comprehensive analysis of the TOM1 homologues based on phylogeny from the most ancient to the youngest representatives within the plant kingdom, analysis of support for tobamovirus accumulation and interaction with other host and viral proteins has not been reported. In this study, using Nicotiana benthamiana and TMV as a model system, we functionally characterized the TOM1 homologues from N. benthamiana and other plant species from different plant lineages. We modified a multiplex genome editing tool and generated a sextuple mutant in which TMV multiplication was dramatically inhibited. We showed that TOM1 homologues from N. benthamiana exhibited variable capacities to support TMV multiplication. Evolutionary analysis revealed that the TOM1 family is restricted to the plant kingdom and probably originated in the Chlorophyta division, suggesting an ancient origin of the TOM1 family. We found that the TOM1 family acquired the ability to promote TMV multiplication after the divergence of moss and spikemoss. Moreover, the capacity of TOM1 orthologues from different plant species to promote TMV multiplication and the interactions between TOM1 and TOM2A and between TOM1 and TMV-encoded replication proteins are highly conserved, suggesting a conserved nature of the TOM2A-TOM1-TMV Hel module in promoting TMV multiplication. Our study not only revealed a conserved nature of a gene module to promote tobamovirus multiplication, but also provides a valuable strategy for TMV-resistant crop development.

Identifiants

pubmed: 37443447
doi: 10.1111/mpp.13375
pmc: PMC10576174
doi:

Substances chimiques

Plant Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1385-1399

Informations de copyright

© 2023 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd.

Références

Mol Plant Microbe Interact. 2020 Nov;33(11):1253-1264
pubmed: 32808862
J Virol. 2003 Aug;77(15):8181-6
pubmed: 12857886
Mol Plant Pathol. 2019 Nov;20(11):1588-1601
pubmed: 31286679
Mol Plant Microbe Interact. 2008 Aug;21(8):1015-26
pubmed: 18616398
Proc Natl Acad Sci U S A. 1982 Oct;79(19):5818-22
pubmed: 6964389
J Virol. 2002 Mar;76(5):2491-7
pubmed: 11836427
J Gen Virol. 2012 Feb;93(Pt 2):408-418
pubmed: 22049092
Methods Mol Biol. 1995;49:39-48
pubmed: 8563823
Mol Plant Pathol. 2023 Nov;24(11):1385-1399
pubmed: 37443447
Philos Trans R Soc Lond B Biol Sci. 1999 Mar 29;354(1383):593-602
pubmed: 10212939
Mol Plant Microbe Interact. 2017 Jan;30(1):5-15
pubmed: 27925500
EMBO J. 2003 Jan 15;22(2):344-53
pubmed: 12514140
Curr Opin Plant Biol. 2012 Aug;15(4):400-6
pubmed: 22445191
Mol Plant Pathol. 2022 Sep;23(9):1278-1289
pubmed: 35706371
Plant J. 2021 Apr;106(1):8-22
pubmed: 33577114
Front Plant Sci. 2014 Nov 21;5:660
pubmed: 25484888
FEBS Lett. 2005 Aug 15;579(20):4479-84
pubmed: 16081069
Intervirology. 1980;14(2):101-8
pubmed: 7203970
Proc Natl Acad Sci U S A. 2000 Aug 29;97(18):10107-12
pubmed: 10944200
Virology. 2020 Aug;547:57-71
pubmed: 32560905
Plant Physiol. 2021 Dec 4;187(4):2674-2690
pubmed: 34636879
Plant Physiol. 2022 Jun 1;189(2):679-686
pubmed: 35262730
J Gen Virol. 2006 Aug;87(Pt 8):2397-2401
pubmed: 16847136
Arch Virol. 2018 May;163(5):1357-1362
pubmed: 29411138
Plant Cell Physiol. 2006 Mar;47(3):426-31
pubmed: 16381658
Plant J. 2002 May;30(4):415-29
pubmed: 12028572
PLoS Pathog. 2012;8(10):e1002975
pubmed: 23093939
Mol Plant Microbe Interact. 2004 Jun;17(6):583-92
pubmed: 15195941
Methods Mol Biol. 2009;479:217-33
pubmed: 19083185
Virus Evol. 2015 Dec 16;1(1):vev019
pubmed: 27774289
Mol Plant Pathol. 2011 Dec;12(9):938-54
pubmed: 22017770
J Virol. 2001 Sep;75(18):8831-6
pubmed: 11507227
Mol Plant Microbe Interact. 2010 Nov;23(11):1413-9
pubmed: 20636106
Front Plant Sci. 2022 Sep 02;13:968855
pubmed: 36119566
Trends Microbiol. 2020 Jan;28(1):46-56
pubmed: 31597598
Mol Plant. 2017 Mar 6;10(3):530-532
pubmed: 28089950
Front Plant Sci. 2022 Mar 03;13:805633
pubmed: 35310653
Proc Natl Acad Sci U S A. 2015 Mar 17;112(11):3570-5
pubmed: 25733849
J Zhejiang Univ Sci B. 2007 Apr;8(4):256-9
pubmed: 17444600
Annu Rev Phytopathol. 2016 Aug 4;54:55-78
pubmed: 27296148
Nucleic Acids Res. 2015 Jul 1;43(W1):W401-7
pubmed: 25969446
Nucleic Acids Res. 1988 Oct 25;16(20):9877
pubmed: 3186459
EMBO J. 2003 Jan 15;22(2):335-43
pubmed: 12514139

Auteurs

Hui Zhang (H)

National Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, China.

Qun Hu (Q)

National Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, China.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Animals Hemiptera Insect Proteins Phylogeny Insecticides
Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family

Classifications MeSH