Abstract
Broad bean wilt virus 1 (BBWV-1, genus Fabavirus, family Secoviridae) infects many plants species, including important horticultural crops. Since some tobacco plants such as Nicotiana benthamiana, are susceptible to many viruses, they are used as experimental hosts and therefore abundant information about these species is available in databases. Here, the protein differential expression in N. benthamiana plants infected with BBWV-1 was studied using Liquid Chromatography coupled with Mass Spectrometry in tandem analysis (LC–MS/MS). Also, we studied the role of viral VP37 protein which is a BBWV-1 determinant of pathogenicity in the accumulation of the host proteins. For this purpose, we agroinfiltrated N. benthamiana plants with two BBWV-1 cDNA infectious clones: pBBWV1-Wt wilt type and the pBBWV1-G492C mutant knocking out for the viral VP37 protein. Virus infection induced the differential expression of 44 host proteins: 22 were overexpressed and the other 22 were underexpressed. These proteins were involved in important plant processes and located in different cell organelles, mainly in chloroplasts. Finally, 24 of these proteins were expressed differentially according to the presence of VP37 protein. Relation among host proteins that were differentially expressed, plant symptoms, and subcellular alterations are discussed.
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References
Agut, B., Gamir, J., Jaques, J. A., & Flors, V. (2016). Systemic resistance in citrus to Tetranychus urticae induced by conspecifics is transmitted by grafting and mediated by mobile amino acids. Journal of Experimental Botany, 67, 5711–5723. https://doi.org/10.1093/jxb/erw335
Albers, S., Czech, A., Ribas De Pouplana, L., & Torres, A. G. (2016). Exploiting tRNAs to boost virulence. Life, 6, 4–6. https://doi.org/10.3390/LIFE6010004
Ali Fayez, K., & Younis Mahmoud, S. (2011). Detection and partial characterization of a putative closterovirus affecting Ficus carica: Molecular, ultrastructural and physiological aspects of infected leaves. Acta Physiologiae Plantarum, 33, 2187–2198. https://doi.org/10.1007/s11738-011-0758-0
Bahir, I., Fromer, M., Prat, Y., & Linial, M. (2009). Viral adaptation to host: A proteome-based analysis of codon usage and amino acid preferences. Molecular Systems Biology, 5, 311. https://doi.org/10.1038/msb.2009.71
Brizard, J. P., Carapito, C., Delalande, F., van Dorsselaer, A., & Brugidou, C. (2006). Proteome analysis of plant-virus interactome: comprehensive data for virus multiplication inside their hosts. Molecular & Cellular Proteomics, 5, 2279–2297. M600173-MCP200.
Carli, M., Benvenuto, E., & Donini, M. (2012). Recent insights into plant−virus interactions through proteomic analysis. Journal of Proteome Research, 10–11, 4765–4780. https://doi.org/10.1021/pr300494e
Carpino, C., Ferriol, I., Elvira-González, L., Rubio, L., Peri, E., Davino, S., et al. (2020b). Broad bean wilt virus 1 encoded VP47 and SCP are suppressors of plant post-transcriptional gene silencing. European Journal of Plant Pathology, 158, 1043–1049. https://doi.org/10.1007/s10658-020-02117-3
Carpino, C., Ferriol I., Elvira‐González, L., Medina, V., Rubio, L., Peri, E., et al. (2020a) RNA2‐encoded VP37 protein of Broad bean wilt virus 1 is a determinant of pathogenicity, host susceptibility, and a suppressor of post‐transcriptional gene silencing. Molecular Plant Pathology, mpp.12979. https://doi.org/10.1111/mpp.12979.
Cerna, H., Černý, M., Habánová, H., Šafářová, D., Abushamsiya, K., Navrátil, M., et al. (2017). Proteomics offers insight to the mechanism behind Pisum sativum L. response to pea seed-borne mosaic virus (PSbMV). Journal of Proteomics, 153, 78–88. https://doi.org/10.1016/J.JPROT.2016.05.018
Chan, Z. (2012). Expression profiling of ABA pathway transcripts indicates crosstalk between abiotic and biotic stress responses in Arabidopsis. Genomics, 100, 110–115. https://doi.org/10.1016/j.ygeno.2012.06.004
Chen, X., & Bruening, G. (1992). Nucleotide sequence and genetic map of cowpea severe mosaic virus RNA 2 and comparisons with RNA 2 of other comoviruses. Virology, 187, 682–692. https://doi.org/10.1016/0042-6822(92)90471-Z
Cho, Y.-H., & Yoo, S.-D. (2011). Signaling role of fructose mediated by FINS1/FBP in Arabidopsis thaliana. PLoS Genetics, 7, e1001263. https://doi.org/10.1371/journal.pgen.1001263
Cui, L., Lu, H., & Lee, Y. H. (2018). Challenges and emergent solutions for LC-MS/MS based untargeted metabolomics in diseases. Mass Spectrometry Reviews, 37, 772–792. https://doi.org/10.1002/MAS.21562
Dang, M., Cheng, Q., Hu, Y., Wu, J., Zhou, X. & Qian, Y. (2020) Proteomic changes during MCMV infection revealed by iTRAQ quantitative proteomic analysis in maize. International Journal of Molecular Sciences, 21. https://doi.org/10.3390/ijms21010035.
Ferriol, I., Rubio, L., Pérez-Panadés, J., Carbonell, E. A., Davino, S., & Belliure, B. (2013). Transmissibility of Broad bean wilt virus 1 by aphids: Influence of virus accumulation in plants, virus genotype and aphid species. Annals of Applied Biology, 162, 71–79. https://doi.org/10.1111/j.1744-7348.2012.00579.x
Gomaa, A., & Boye, J. (2015). Simultaneous detection of multi-allergens in an incurred food matrix using ELISA, multiplex flow cytometry and liquid chromatography mass spectrometry (LC–MS). Food Chemistry, 175, 585–592. https://doi.org/10.1016/J.FOODCHEM.2014.12.017
Harries, P. A., Park, J. W., Sasaki, N., Ballard, K. D., Maule, A. J., & Nelson, R. S. (2009). Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proceedings of the National Academy of Sciences of the United States of America, 106, 17594–17599. https://doi.org/10.1073/PNAS.0909239106
Jain, A., Singh, H. B., & Das, S. (2021). Deciphering plant-microbe crosstalk through proteomics studies. Microbiological Research, 242, 125690. https://doi.org/10.1016/j.micres.2020.126590
Jones, R. A. C. (2021). Global plant virus disease pandemics and epidemics. Plants 2021, 10, 233–233. https://doi.org/10.3390/PLANTS10020233
King, A.M.Q., Lefkowitz, E., Adams, M.J. & Carstens, E.B. (2011). Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier. ISBN: 978-0-12-384684-6.
Lekkerkerker, A., Wellink, J., Yuan, P., van Lent, J., Goldbach, R., & van Kammen, A. B. (1996). Distinct functional domains in the cowpea mosaic virus movement protein. Journal of Virology, 70, 5658–5661. https://doi.org/10.1128/jvi.70.8.5658-5661.1996
Lidia, A., Varela, N., Komatsu, S., Wang, X., Silva, R. G. G., Filho, P., et al. (2017). Gel-free/label-free proteomic, photosynthetic, and biochemical analysis of cowpea (Vigna unguiculata [L.] Walp.) resistance against Cowpea severe mosaic virus (CPSMV). Journal of Proteomics, 163, 76–91. https://doi.org/10.1016/j.jprot.2017.05.003
Martínez, C., Coll-Bonfill, N., Aramburu, J., Pallás, V., Aparicio, F., & Galipienso, L. (2014). Two basic (hydrophilic) regions in the movement protein of Parietaria mottle virus have RNA binding activity and are required for cell-to-cell transport. Virus Research, 184, 54–61. https://doi.org/10.1016/j.virusres.2014.02.008
Medina, V., Carpino, C., Elvira-González, L., Rubio, L., & Galipienso, L. (2022). Subcellular effects of broad bean wilt virus 1 infection in Nicotiana benthamiana and broad bean plants. European Journal of Plan Pathology, 164, 451–459. https://doi.org/10.1007/s10658-022-02564-0
Mittapelly, P., & Rajarapu, S. P. (2020). Applications of proteomic tools to study insect vector–plant virus interactions. Life, 10, 143. https://doi.org/10.3390/LIFE10080143
Nazarov, P. A., Baleev, D. N., Ivanova, M. I., Sokolova, L. M., & Karakozova, M. V. (2020). Infectious plant diseases: etiology, current status, problems and prospects in plant protection. Acta Naturae, 12, 46. https://doi.org/10.32607/ACTANATURAE.11026
Palukaitis, P., & García-Arenal, F. (2003). Cucumoviruses. Advances in Virus Research, 62(2), 41–323. https://doi.org/10.1016/s0065-3527(03)62005-1
Qi, Y. J., Zhou, X. P., Huang, X. Z., & Li, G. X. (2002). In vivo accumulation of Broad bean wilt virus 2 VP37 protein and its ability to bind single-stranded nucleic acid. Archives of Virology, 147, 917–928. https://doi.org/10.1007/s00705-001-0782-2
Šafářová, D., Faure, C., Marais, A., Suchá, J., Paprštein, F., Navrátil, M., et al. (2017). First report of prunus virus F infecting sour cherry in the Czech Republic. Plant Disease, 101, 1828. https://doi.org/10.1094/PDIS-04-17-0469-PDN
Sanfaçon, H. (2017). Grand challenge in plant virology: Understanding the impact of plant viruses in model plants, in agricultural crops, and in complex ecosystems. Frontiers in Microbiology, 8, 860. https://doi.org/10.3389/FMICB.2017.00860/BIBTEX
Sanfaçon, H. (2015) Secoviridae: A Family of Plant Picorna‐Like Viruses with Monopartite or Bipartite Genomes. eLS. https://doi.org/10.1002/9780470015902.a0000764.pub3.
Shilov, I. V., Seymour, S. L., Patel, A. A., Loboda, A., Tang, W. H., Keating, S. P., Hunter, C. L., Nuwaysir, L. M., & Schaeffer, D. A. (2007). The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Molecular & Cellular Proteomics, 6, 1638–1655. https://doi.org/10.1074/mcp.T600050-MCP200
Souza, P. F. N., Garcia-Ruiz, H., & Carvalho, F. E. L. (2019). What proteomics can reveal about plant–virus interactions? Photosynthesis-related proteins on the spotlight. Theoretical and Experimental Plant Physiology, 31, 227–248. https://doi.org/10.1007/s40626-019-00142-0
Varela, A. L. N., Komatsu, S., Wang, X., Silva, R. G. G., Souza, P. F. N., Lobo, A. K. M., et al. (2017). Gel-free/label-free proteomic, photosynthetic, and biochemical analysis of cowpea (Vigna unguiculata [L.] Walp.) resistance against Cowpea severe mosaic virus (CPSMV). Journal of Proteomics, 163, 76–91. https://doi.org/10.1016/J.JPROT.2017.05.003
Varela, A. L. N., Oliveira, J. T. A., Komatsu, S., Silva, R. G. G., Martins, T. F., Souza, P. F. N., et al. (2019). A resistant cowpea (Vigna unguiculata [L.] Walp.) genotype became susceptible to cowpea severe mosaic virus (CPSMV) after exposure to salt stress. Journal of Proteomics, 194, 200–217. https://doi.org/10.1016/j.jprot.2018.11.015
Wagaba, H., Beyene, G., Aleu, J., Odipio, J., Okao-Okuja, G., Chauhan, R. D., et al. (2017). Field level RNAi-mediated resistance to cassava brown streak disease across multiple cropping cycles and diverse east African agro-ecological locations. Frontiers in Plant Science, 7, 2060. https://doi.org/10.3389/FPLS.2016.02060/BIBTEX
Wan, J., & Laliberté, J. F. (2015). Membrane-associated virus replication complexes locate to plant conducting tubes. Plant Signaling & Behaviour, 10, 8. https://doi.org/10.1080/15592324.2015.1042639
Wang, B., Hajano, J. U. D., Ren, Y., Lu, C., & Wang, X. (2015). iTRAQ-based quantitative proteomics analysis of rice leaves infected by Rice stripe virus reveals several proteins involved in symptom formation. Virology Journal, 12, 1–21. https://doi.org/10.1186/S12985-015-0328-Y/FIGURES/7
Wang, J., Wang, X. R., Zhou, Q., Yang, J. M., Guo, H. X., Yang, L. J., et al. (2016). iTRAQ protein profile analysis provides integrated insight into mechanisms of tolerance to TMV in tobacco (Nicotiana tabacum). Journal of Proteomics, 132, 21–30. https://doi.org/10.1016/J.JPROT.2015.11.009
Xie, L., Shang, W., Liu, C., Zhang, Q., Sunter, G., Hong, J., et al. (2016). Mutual association of Broad bean wilt virus 2 VP37-derived tubules and plasmodesmata obtained from cytological observation. Scientific Reports, 6, 21552. https://doi.org/10.1038/srep21552
Yang, X., Lu, Y., Wang, F., Chen, Y., Tian, Y., Jiang, L., et al. (2020). Involvement of the chloroplast gene ferredoxin 1 in multiple responses of Nicotiana benthamiana to Potato virus X infection. Journal of Experimental Botany, 71, 2142–2156. https://doi.org/10.1093/JXB/ERZ565
Zechmann, B., Müller, M., Möstl, S., & Zellnig, G. (2021). Three-dimensional quantitative imaging of Tobacco mosaic virus and Zucchini yellow mosaic virus induced ultrastructural changes. Protoplasma, 258, 1201–1211. https://doi.org/10.1007/s00709-021-01626-0/Published
Zeeman, S. C., Kossmann, J., & Smith, A. M. (2010). Starch: Its metabolism, evolution, and biotechnological modification in plants. Annual Reviews of Plant Biology, 61, 209–234. https://doi.org/10.1146/ANNUREV-ARPLANT-042809-112301
Zeier, J. (2013). New insights into the regulation of plant immunity by amino acid metabolic pathways. Plant, Cell & Environment, 36, 2085–2103. https://doi.org/10.1111/pce.12122
Zhan, J., Shi, H., Li, W., Zhang, C., & Zhang, Y. (2021). NbTMP14 is involved in Tomato spotted wilt virus infection and symptom development by interaction with the viral NSm protein. Viruses, 13, 427–427. https://doi.org/10.3390/V13030427
Zhang, Q., Zhang, Y., Wang, S., Hao, L., Wang, S., Xu, C., et al. (2019). Characterization of genome-wide microRNAs and their roles in development and biotic stress in pear. Planta, 249, 693–707. https://doi.org/10.1007/s00425-018-3027-2
Acknowledgements
We thank Dr. Leonardo Velasco for the critical review of the manuscript. Proteomic and biostatistical analysis were conducted by the proteomics unit of the Universitat de València.
Funding
This research work was supported by funds of the Instituto Valenciano de Investigaciones Agrarias, Valencia, Spain (PROY-IVIA-2013/14 n 5426). C. Carpino was a recipient of predoctoral fellowships from the Italian government.
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C. Carpino and L. Elvira-González prepared the plant material for proteomic analysis. L. Elvira-González is responsible of the experimental analysis and the manuscript writing. L. Galipienso conducted the experimental design, the manuscript revision and edition. Luis Rubio participated in the manuscript revision and edition.
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Elvira-González, L., Carpino, C., Rubio, L. et al. Proteomic insights into the effect of Broad bean wilt virus-1 infection in Nicotiana benthamiana plants. Eur J Plant Pathol (2023). https://doi.org/10.1007/s10658-023-02802-z
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DOI: https://doi.org/10.1007/s10658-023-02802-z