The miR172/TOE3 module regulates resistance to tobacco mosaic virus in tobacco.
Nicotiana tabacum
defense‐related gene
miR172/TOE3
symptom recovery
tobacco mosaic virus
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
23 Jul 2024
23 Jul 2024
Historique:
revised:
01
07
2024
received:
18
04
2024
accepted:
04
07
2024
medline:
23
7
2024
pubmed:
23
7
2024
entrez:
23
7
2024
Statut:
aheadofprint
Résumé
The outcome of certain plant-virus interaction is symptom recovery, which is accompanied with the emergence of asymptomatic tissues in which the virus accumulation decreased dramatically. This phenomenon shows the potential to reveal critical molecular factors for controlling viral disease. MicroRNAs act as master regulators in plant growth, development, and immunity. However, the mechanism by which miRNA participates in regulating symptom recovery remains largely unknown. Here, we reported that miR172 was scavenged in the recovered tissue of tobacco mosaic virus (TMV)-infected Nicotiana tabacum plants. Overexpression of miR172 promoted TMV infection, whereas silencing of miR172 inhibited TMV infection. Then, TARGET OF EAT3 (TOE3), an APETALA2 transcription factor, was identified as a downstream target of miR172. Overexpression of NtTOE3 significantly improved plant resistance to TMV infection, while knockout of NtTOE3 facilitated virus infection. Furthermore, transcriptome analysis indicated that TOE3 promoted the expression of defense-related genes, such as KL1 and MLP43. Overexpression of these genes conferred resistance of plant against TMV infection. Importantly, results of dual-luciferase assay, chromatin immunoprecipitation-quantitative PCR, and electrophoretic mobility shift assay proved that TOE3 activated the transcription of KL1 and MLP43 by binding their promoters. Moreover, overexpression of rTOE3 (the miR172-resistant form of TOE3) significantly reduced TMV accumulation compared to the overexpression of TOE3 (the normal form of TOE3) in miR172 overexpressing Nicotiana benthamiana plants. Taken together, our study reveals the pivotal role of miR172/TOE3 module in regulating plant immunity and in the establishment of recovery in virus-infected tobacco plants, elucidating a regulatory mechanism integrating plant growth, development, and immune response.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Natural Science Foundation of China
ID : 32270166
Organisme : National Natural Science Foundation of China
ID : 32070167
Organisme : Fundamental Research Funds for the Central Universities
ID : 2022SCUH0006
Organisme : Natural Science Foundation of Sichuan Province
ID : 2023NSFSC0148
Informations de copyright
© 2024 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Arora, S., Pandey, D.K. & Chaudhary, B. (2019) Target‐mimicry based diminution of miRNA167 reinforced flowering‐time phenotypes in tobacco via spatial‐transcriptional biases of flowering‐associated miRNAs. Gene, 682, 67–80.
Aukerman, M.J. & Sakai, H. (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2‐like target genes. The Plant Cell, 15, 2730–2741.
Boualem, A., Dogimont, C. & Bendahmane, A. (2016) The battle for survival between viruses and their host plants. Current Opinion in Virology, 17, 32–38.
Cao, Z., Ma, X.Z., Lv, D.S., Wang, J., Shen, Y., Peng, S.Q. et al. (2023) Synthesis of chitin nanocrystals supported Zn2+ with high activity against tobacco mosaic virus. International Journal of Biological Macromolecules, 250, 126168.
Chen, L.J., Zhao, F.F., Zhang, M., Lin, H.H. & Xi, D.H. (2015) Characterisation of the dark green islands of cucumber mosaic virus infected Nicotiana tabacum. Plant Cell Reports, 34, 1225–1238.
Chen, X.M. (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science, 303, 2022–2025.
Cheng, X.L., He, Q., Tang, S., Wang, H.R., Zhang, X.X., Lv, M.J. et al. (2021) The miR172/IDS1 signaling module confers salt tolerance through maintaining ROS homeostasis in cereal crops. New Phytologist, 230, 1017–1033.
Cheng, X.L., Zhang, S.X., Tao, W.C., Zhang, X.X., Liu, J., Sun, J.Q. et al. (2018) INDETERMINATE SPIKELET1 recruits histone deacetylase and a transcriptional repression complex to regulate rice salt tolerance. Plant Physiology, 178, 824–837.
Deng, Y.T., Wang, J.B., Tung, J., Liu, D., Zhou, Y.J., He, S. et al. (2018) A role for small RNA in regulating innate immunity during plant growth. PLoS Pathogen, 14, e1006756.
Dinh, T.T., Girke, T., Liu, X.G., Yant, L., Schmid, M. & Chen, X.M. (2012) The floral homeotic protein APETALA2 recognizes and acts through an AT‐rich sequence element. Development, 139, 1978–1986.
Fei, Q.L., Xia, R. & Meyers, B.C. (2013) Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. The Plant Cell, 25, 2400–2415.
Feng, Q., Wang, H., Yang, X.M., Hu, Z.W., Zhou, X.H., Xiang, L. et al. (2022) Osa‐miR160a confers broad‐spectrum resistance to fungal and bacterial pathogens in rice. New Phytologist, 236, 2216–2232.
Ghoshal, B. & Sanfaçon, H. (2015) Symptom recovery in virus‐infected plants: revisiting the role of RNA silencing mechanisms. Virology, 479, 167–179.
Han, H.Y., Zou, J.L., Zhou, J.Y., Zeng, M.Y., Zheng, D.C., Yuan, X.F. et al. (2022) The small GTPase NtRHO1 negatively regulates tobacco defense response to tobacco mosaic virus by interacting with NtWRKY50. Journal of Experimental Botany, 73, 366–381.
Han, Y.Y., Zhang, X., Wang, Y.F. & Ming, F. (2013) The suppression of WRKY44 by GIGANTEA‐miR172 pathway is involved in drought response of Arabidopsis thaliana. PLoS One, 8, e73541.
He, Z.H., Webster, S. & He, S.Y. (2022) Growth–defense trade‐offs in plants. Current Biology, 32, R589–R683.
Jin, Y., Zhao, J.H. & Guo, H.S. (2021) Recent advances in understanding plant antiviral RNAi and viral suppressors of RNAi. Current Opinion in Virology, 46, 65–72.
Jung, J.H., Seo, Y.H., Seo, P.J., Reyes, J.L., Yun, J., Chua, N.H. et al. (2007) The GIGANTEA‐regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. The Plant Cell, 19, 2736–2748.
Korner, C.J., Pitzalis, N., Peña, E.J., Erhardt, M., Vazquez, F. & Heinlein, M. (2018) Crosstalk between PTGS and TGS pathways in natural antiviral immunity and disease recovery. Nature Plants, 4, 157–164.
Lee, Y.S., Lee, D.Y., Cho, L.H. & An, G. (2014) Rice miR172 induces flowering by suppressing OsIDS1 and SNB, two AP2 genes that negatively regulate expression of Ehd1 and florigens. Rice, 7, 31.
Leonetti, P., Stuttmann, J. & Pantaleo, V. (2021) Regulation of plant antiviral defense genes via host RNA‐silencing mechanisms. Virology Journal, 18, 194.
Li, F., Pignatta, D., Bendix, C., Brunkard, J.O., Cohn, M.M., Tung, J. et al. (2012) MicroRNA regulation of plant innate immune receptors. Proceedings of the National Academy of Sciences of the United States of America, 109, 1790–1795.
Li, Y., Lu, Y.G., Shi, Y., Wu, L., Xu, Y.J., Huang, F. et al. (2014) Multiple rice microRNAs are involved in immunity against the blast fungus. Plant Physiology, 164, 1077–1092.
Li, Y., Zhang, Q., Zhang, J., Wu, L., Qi, Y. & Zhou, J.M. (2010) Identification of microRNAs involved in pathogen‐associated molecular pattern‐triggered plant innate immunity. Plant Physiology, 152, 2222–2231.
Lin, K.Y., Wu, S.Y., Hsu, Y.H. & Lin, N.S. (2022) MiR398‐regulated antioxidants contribute to bamboo mosaic virus accumulation and symptom manifestation. Plant Physiology, 188, 593–607.
Liu, S., Chen, M.J., Li, R.D., Li, W.X., Gal‐On, A., Jia, Z.Y. et al. (2022) Identification of positive and negative regulators of antiviral RNA interference in Arabidopsis thaliana. Nature Communications, 13, 2994.
Malavka, M., Prakash, V. & Chakraborty, S. (2023) Recovery from virus infection: plant's armory in action. Planta, 257, 103.
Mengistu, A.A. & Tenkegna, T.A. (2021) The role of miRNA in plant‐virus interaction: a review. Molecular Biology Reports, 48, 2853–2861.
Namgial, T., Singh, A.K., Singh, N.P., Francis, A., Chattopadhyay, D., Voloudakis, A. et al. (2023) Differential expression of genes during recovery of Nicotiana tabacum from tomato leaf curl gujarat virus infection. Planta, 258, 37.
Naqvi, A.R., Haq, Q.M.R. & Mukherjee, S.K. (2010) MicroRNA profiling of Tomato leaf curl New Delhi virus (ToLCNDV) infected tomato leaves indicates that deregulation of miR159/319 and miR172 might be linked with leaf curl disease. Virology Journal, 7, 281.
Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M. et al. (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science, 312, 436–439.
Park, W., Li, J.J., Song, R.T., Messing, J. & Chen, X.M. (2002) CARPEL FACTORY, a dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Current Biology, 12, 1484–1495.
Peng, Q.D., Jiao, B.L., Cheng, Y.C., Yuan, B.W., Zhou, J.Y., Cai, J.L. et al. (2024) NtG3BPL1 confers resistance to chilli veinal mottle virus through promoting the degradation of 6K2 in tobacco. The Plant Journal, 119, 720–734.
Peng, Q.D., Yang, D.Y., Yang, T., Cheng, Y.C., Yang, Y.F. & Xi, D.H. (2022) Construction of full‐length cDNA infectious clones of Chilli veinal mottle virus. Virus Research, 322, 198948.
Sahito, Z.A., Wang, L.X., Sun, Z.X., Yan, Q.Q., Zhang, X.K., Jiang, Q. et al. (2017) The miR172c‐NNC1 module modulates root plastic development in response to salt in soybean. BMC Plant Biology, 17, 229.
Sharma, N., Sahu, P.P., Prasad, A., Muthamilarasan, M., Waseem, M., Khan, Y. et al. (2021) The Sw5a gene confers resistance to ToLCNDV and triggers an HR response after direct AC4 effector recognition. Proceedings of the National Academy of Sciences of the United States of America, 118, e2101833118.
Sierro, N., Battey, J.N.D., Ouadi, S., Bakaher, N., Bovet, L., Willig, A. et al. (2014) The tobacco genome sequence and its comparison with those of tomato and potato. Nature Communications, 5, 3833.
Song, L.Y., Jiao, Y.B., Song, H.P., Shao, Y.Z., Zhang, D.S., Ding, C.Y. et al. (2023) NbMLP43 ubiquitination and proteasomal degradation via the light responsive factor NbBBX24 to promote viral infection. Cells, 12, 590.
Song, X.W., Li, Y., Cao, X.F. & Qi, Y.J. (2019) MicroRNAs and their regulatory roles in plant‐environment interactions. Annual Review of Plant Biology, 70, 489–525.
Tang, J.Y. & Chu, C.C. (2017) MicroRNAs in crop improvement: fine‐tuners for complex traits. Nature Plants, 3, 17077.
Tong, X., Zhao, J.J., Feng, Y.L., Zou, J.Z., Ye, J., Liu, J. et al. (2023) A selective autophagy receptor VISP1 induces symptom recovery by targeting viral silencing suppressors. Nature Communications, 14, 3852.
Wang, T.Y., Ping, X.K., Cao, Y.R., Jian, H.J., Gao, Y.M., Wang, J. et al. (2019) Genome‐wide exploration and characterization of miR172/euAP2 genes in Brassica napus L. for likely role in flower organ development. BMC Plant Biology, 19, 336.
Wang, Z.M., Hardcastle, T.J., Canto, P.A., Yip, W.H., Tang, S.Y. & Baulcombe, D.C. (2018) A novel DCL2‐dependent miRNA pathway in tomato affects susceptibility to RNA viruses. Genes and Development, 32, 1155–1160.
Wei, Y.X., Xie, H.Q., Xu, L.L., Cheng, X., Zhu, B.B., Zheng, H.Q. et al. (2024) Coat protein of cassava common mosaic virus targets RAV1 and RAV2 transcription factors to subvert immunity in cassava. Plant Physiology, 194, 1218–1232.
Yan, J., Gu, Y.Y., Jia, X.Y., Kang, W.J., Pan, S.J., Tang, X.Q. et al. (2012) Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. The Plant Cell, 24, 415–427.
Yang, T., Qiu, L., Huang, W.Y., Xu, Q.Y., Zou, J.L., Peng, Q.D. et al. (2020) Chilli veinal mottle virus HCPro interacts with catalase to facilitate virus infection in Nicotiana tabacum. Journal of Experimental Botany, 71, 5656–5668.
Yuan, M.H., Jiang, Z.Y., Bi, G.Z., Nomura, K., Liu, M.H., Wang, Y.P. et al. (2021) Pattern‐recognition receptors are required for NLR‐mediated plant immunity. Nature, 592, 105–109.
Zeng, M.Y., Jiao, B.L., Liu, S.C., Yang, Y.F., Peng, Q.D., Huang, W.Y. et al. (2023) HCPro affects heterologous virus infection through salicylic acid and auxin pathways. Plant Pathology, 72, 1416–1427.
Zhang, C., Ding, Z.M., Wu, K.C., Yang, L., Li, Y., Yang, Z. et al. (2016) Suppression of jasmonic acid‐mediated defense by viral‐inducible microRNA319 facilitates virus infection in rice. Molecular Plant, 9, 1302–1314.
Zhang, H., Wang, Z., Li, X., Gao, X.R., Dai, Z.R., Cui, Y.F. et al. (2021) The IbBBX24–IbTOE3–IbPRX17 module enhances abiotic stress tolerance by scavenging reactive oxygen species in sweet potato. New Phytologist, 233, 1133–1152.
Zhang, T.T., Tang, Y.H., Luan, Y.T., Cheng, Z.Y., Wang, X.X., Tao, J. et al. (2022) Herbaceous peony AP2/ERF transcription factor binds the promoter of the tryptophan decarboxylase gene to enhance high‐temperature stress tolerance. Plant, Cell & Environment, 45, 2729–2743.
Zhang, X.P., Liu, D.S., Yan, T., Fang, X.D., Dong, K., Xu, J. et al. (2017) Cucumber mosaic virus coat protein modulates the accumulation of 2b protein and antiviral silencing that causes symptom recovery in planta. PLoS Pathogens, 13, e1006522.
Zhao, F.F., Li, Y.N., Chen, L.J., Zhu, L.S., Ren, H., Lin, H.H. et al. (2016) Temperature dependent defence of Nicotiana tabacum against cucumber mosaic virus and recovery occurs with the formation of dark green islands. Journal Of Plant Biology, 59, 293–301.
Zhou, J.Y., Han, H.Y., Liu, S.C., Ji, C.L., Jiao, B.L., Yang, Y.T. et al. (2024) miRNAs are involved in regulating the formation of recovery tissues in virus infected Nicotiana tabacum. Molecular Genetics and Genomics, 299, 10.
Zhu, Q.H., Jin, S.X., Yuan, Y.M., Liu, Q., Zhang, X.L. & Wilson, I. (2022) CRISPR/Cas9‐mediated saturated mutagenesis of the cotton MIR482 family for dissecting the functionality of individual members in disease response. Plant Direct, 6, e410.
Zou, Y.M., Wang, S.F. & Lu, D.P. (2020) MiR172b‐TOE1/2 module regulates plant innate immunity in an age‐dependent manner. Biochemical and Biophysical Research Communications, 531, 503–507.
Zou, Y.M., Wang, S.F., Zhou, Y.Y., Bai, J.J., Huang, G.Z., Liu, X.T. et al. (2018) Transcriptional regulation of the immune receptor FLS2 controls the ontogeny of plant innate immunity. The Plant Cell, 30, 2779–2794.
Zou, Y.M., Wang, Y.N., Wang, L.X., Yang, L., Wang, R. & Li, X. (2013) MiR172b controls the transition to autotrophic development inhibited by ABA in Arabidopsis. PLoS One, 8, e64770.
Zumajo‐Cardona, C. & Pabón‐Mora, N. (2016) Evolution of the APETALA2 gene lineage in seed plants. Molecular Biology and Evolution, 33, 1818–1832.