Transgenic expression of artificial microRNA targeting soybean mosaic virus P1 gene confers virus resistance in plant.
P1 gene
MicroRNA
Potyvirus
SMV
Transgenic
Virus resistance
Journal
Transgenic research
ISSN: 1573-9368
Titre abrégé: Transgenic Res
Pays: Netherlands
ID NLM: 9209120
Informations de publication
Date de publication:
06 Jun 2024
06 Jun 2024
Historique:
received:
28
02
2024
accepted:
28
05
2024
medline:
6
6
2024
pubmed:
6
6
2024
entrez:
6
6
2024
Statut:
aheadofprint
Résumé
RNA silencing is an innate immune mechanism of plants against invasion by viral pathogens. Artificial microRNA (amiRNA) can be engineered to specifically induce RNA silencing against viruses in transgenic plants and has great potential for disease control. Here, we describe the development and application of amiRNA-based technology to induce resistance to soybean mosaic virus (SMV), a plant virus with a positive-sense single-stranded RNA genome. We have shown that the amiRNA targeting the SMV P1 coding region has the highest antiviral activity than those targeting other SMV genes in a transient amiRNA expression assay. We transformed the gene encoding the P1-targeting amiRNA and obtained stable transgenic Nicotiana benthamiana lines (amiR-P1-3-1-2-1 and amiR-P1-4-1-2-1). Our results have demonstrated the efficient suppression of SMV infection in the P1-targeting amiRNA transgenic plants in an expression level-dependent manner. In particular, the amiR-P1-3-1-2-1 transgenic plant showed high expression of amiR-P1 and low SMV accumulation after being challenged with SMV. Thus, a transgenic approach utilizing the amiRNA technology appears to be effective in generating resistance to SMV.
Identifiants
pubmed: 38842603
doi: 10.1007/s11248-024-00388-8
pii: 10.1007/s11248-024-00388-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Natural Science Foundation of China
ID : 32370158
Organisme : National Natural Science Foundation of China
ID : 32370158
Organisme : Jiangsu Province's Innovation Program
ID : JSSCTD202142
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Nature Switzerland AG.
Références
Bassett M, Salemi M, Rife Magalis B (2022) Lessons learned and yet-to-be learned on the importance of RNA structure in SARS-CoV-2 replication. Microbiol Mol Biol Rev 86:e0005721. https://doi.org/10.1128/mmbr.00057-21
doi: 10.1128/mmbr.00057-21
pubmed: 35862724
Carbonell A, Lopez C, Daros JA (2019) Fast-forward identification of highly effective artificial small RNAs against different tomato spotted wilt virus isolates. Mol Plant Microbe Interact 32:142–156. https://doi.org/10.1094/MPMI-05-18-0117-TA
doi: 10.1094/MPMI-05-18-0117-TA
pubmed: 30070616
Chatzi A, Doody O (2023) The one-way ANOVA test explained. Nurse Res 31:8–14. https://doi.org/10.7748/nr.2023.e1885
doi: 10.7748/nr.2023.e1885
pubmed: 37317616
Duan CG, Wang CH, Fang RX, Guo HS (2008) Artificial microRNAs highly accessible to targets confer efficient virus resistance in plants. J Virol 82:11084–11095. https://doi.org/10.1128/JVI.01377-08
doi: 10.1128/JVI.01377-08
pubmed: 18768978
pmcid: 2573272
Gallois P, Marinho P (1995) Leaf disk transformation using Agrobacterium tumefaciens-expression of heterologous genes in tobacco. Methods Mol Biol 49:39–48. https://doi.org/10.1385/0-89603-321-X:39
doi: 10.1385/0-89603-321-X:39
pubmed: 8563823
Gao L, Ding X, Li K, Liao W, Zhong Y, Ren R, Liu Z, Adhimoolam K, Zhi H (2015) Characterization of Soybean mosaic virus resistance derived from inverted repeat-SMV-HC-Pro genes in multiple soybean cultivars. Theor Appl Genet 128:1489–1505. https://doi.org/10.1007/s00122-015-2522-0
doi: 10.1007/s00122-015-2522-0
pubmed: 25930057
Hajimorad MR, Domier LL, Tolin SA, Whitham SA, Saghai Maroof MA (2018) Soybean mosaic virus: a successful potyvirus with a wide distribution but restricted natural host range. Mol Plant Pathol 19:1563–1579. https://doi.org/10.1111/mpp.12644
doi: 10.1111/mpp.12644
pubmed: 29134790
pmcid: 6638002
Hong X, Li S, Cheng X, Zhi H, Yin J, Xu K (2024) Searching for plant NLR immune receptors conferring resistance to potyviruses. Crop J 12:28–44. https://doi.org/10.1016/j.cj.2023.11.010
doi: 10.1016/j.cj.2023.11.010
Ishibashi K, Saruta M, Shimizu T, Shu M, Anai T, Komatsu K, Yamada N, Katayose Y, Ishikawa M, Ishimoto M, Kaga A (2019) Soybean antiviral immunity conferred by dsRNase targets the viral replication complex. Nat Commun 10:4033. https://doi.org/10.1038/s41467-019-12052-5
doi: 10.1038/s41467-019-12052-5
pubmed: 31562302
pmcid: 6764979
Jian C, Han R, Chi Q, Wang S, Ma M, Liu X, Zhao H (2017) Virus-based microRNA silencing and overexpressing in common wheat (Triticum aestivum L.). Front Plant Sci 8:500. https://doi.org/10.3389/fpls.2017.00500
doi: 10.3389/fpls.2017.00500
pubmed: 28443107
pmcid: 5385339
Kim HJ, Kim M-J, Pak JH, Im HH, Lee DH, Kim K-H, Lee J-H, Kim D-H, Choi HK, Jung HW, Chung Y-S (2016) RNAi-mediated Soybean mosaic virus (SMV) resistance of a Korean soybean cultivar. Plant Biotechnol Rep 10:257–267. https://doi.org/10.1007/s11816-016-0402-y
doi: 10.1007/s11816-016-0402-y
Kis A, Tholt G, Ivanics M, Varallyay E, Jenes B, Havelda Z (2016) Polycistronic artificial miRNA-mediated resistance to wheat dwarf virus in barley is highly efficient at low temperature. Mol Plant Pathol 17:427–437. https://doi.org/10.1111/mpp.12291
doi: 10.1111/mpp.12291
pubmed: 26136043
Mallory AC, Reinhart BJ, Jones-Rhoades MW, Tang G, Zamore PD, Barton MK, Bartel DP (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5’ region. EMBO J 23:3356–3364. https://doi.org/10.1038/sj.emboj.7600340
doi: 10.1038/sj.emboj.7600340
pubmed: 15282547
pmcid: 514513
Miao S, Liang C, Li J, Baker B, Luo L (2021) Polycistronic artificial microrna-mediated resistance to cucumber green mottle mosaic virus in cucumber. Int J Mol Sci. https://doi.org/10.3390/ijms222212237
doi: 10.3390/ijms222212237
pubmed: 35008888
pmcid: 8745443
Mitter N, Dietzgen RG (2012) Use of hairpin RNA constructs for engineering plant virus resistance. Methods Mol Biol 894:191–208. https://doi.org/10.1007/978-1-61779-882-5_13
doi: 10.1007/978-1-61779-882-5_13
pubmed: 22678581
Park W, Zhai J, Lee JY (2009) Highly efficient gene silencing using perfect complementary artificial miRNA targeting AP1 or heteromeric artificial miRNA targeting AP1 and CAL genes. Plant Cell Rep 28:469–480. https://doi.org/10.1007/s00299-008-0651-5
doi: 10.1007/s00299-008-0651-5
pubmed: 19066901
Qu J, Ye J, Fang R (2007) Artificial microRNA-mediated virus resistance in plants. J Virol 81:6690–6699. https://doi.org/10.1128/JVI.02457-06
doi: 10.1128/JVI.02457-06
pubmed: 17344304
pmcid: 1900123
Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133. https://doi.org/10.1105/tpc.105.039834
doi: 10.1105/tpc.105.039834
pubmed: 16531494
pmcid: 1456875
Simon AE (2015) 3’UTRs of carmoviruses. Virus Res 206:27–36. https://doi.org/10.1016/j.virusres.2015.01.023
doi: 10.1016/j.virusres.2015.01.023
pubmed: 25662021
Szittya G, Silhavy D, Molnar A, Havelda Z, Lovas A, Lakatos L, Banfalvi Z, Burgyan J (2003) Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J 22:633–640. https://doi.org/10.1093/emboj/cdg74
doi: 10.1093/emboj/cdg74
pubmed: 12554663
pmcid: 140757
Varkonyi-Gasic E, Wu R, Wood M, Walton EF, Hellens RP (2007) Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3:12. https://doi.org/10.1186/1746-4811-3-12
doi: 10.1186/1746-4811-3-12
pubmed: 17931426
pmcid: 2225395
Vu TV, Choudhury NR, Mukherjee SK (2013) Transgenic tomato plants expressing artificial microRNAs for silencing the pre-coat and coat proteins of a begomovirus, tomato leaf curl New Delhi virus, show tolerance to virus infection. Virus Res 172:35–45. https://doi.org/10.1016/j.virusres.2012.12.008
doi: 10.1016/j.virusres.2012.12.008
pubmed: 23276684
Xu B, Zhu Y, Cao C, Chen H, Jin Q, Li G, Ma J, Yang SL, Zhao J, Zhu J, Ding Y, Fang X, Jin Y, Kwok CK, Ren A, Wan Y, Wang Z, Xue Y, Zhang H, Zhang QC, Zhou Y (2022) Recent advances in RNA structurome. Sci China Life Sci 65:1285–1324. https://doi.org/10.1007/s11427-021-2116-2
doi: 10.1007/s11427-021-2116-2
pubmed: 35717434
pmcid: 9206424
Yin J, Wang L, Jin T, Nie Y, Liu H, Qiu Y, Yang Y, Li B, Zhang J, Wang D, Li K, Xu K, Zhi H (2021) A cell wall-localized NLR confers resistance to Soybean mosaic virus by recognizing viral-encoded cylindrical inclusion protein. Mol Plant 14:1881–1900. https://doi.org/10.1016/j.molp.2021.07.013
doi: 10.1016/j.molp.2021.07.013
pubmed: 34303025