The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Variability in the Viral Protein Linked to the Genome of Turnip Mosaic Virus Influences Interactions with eIF(iso)4Es in Brassica rapa

  • Li, Guoliang (State Key Laboratory of North China Crop Improvement and Regulation, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences) ;
  • Zhang, Shifan (State Key Laboratory of North China Crop Improvement and Regulation, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences) ;
  • Li, Fei (State Key Laboratory of North China Crop Improvement and Regulation, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences) ;
  • Zhang, Hui (State Key Laboratory of North China Crop Improvement and Regulation, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences) ;
  • Zhang, Shujiang (State Key Laboratory of North China Crop Improvement and Regulation, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences) ;
  • Zhao, Jianjun (State Key Laboratory of North China Crop Improvement and Regulation, Department of Horticulture, Hebei Agricultural University) ;
  • Sun, Rifei (State Key Laboratory of North China Crop Improvement and Regulation, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences)
  • Received : 2020.07.17
  • Accepted : 2020.12.31
  • Published : 2021.02.01
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Abstract

Plants protect against viruses through passive and active resistance mechanisms, and in most cases characterized thus far, natural recessive resistance to potyviruses has been mapped to mutations in the eukaryotic initiation factor eIF4E or eIF(iso)4E genes. Five eIF4E copies and three eIF(iso)4E copies were detected in Brassica rapa. The eIF4E and eIF(iso)4E genes could interact with turnip mosaic virus (TuMV) viral protein linked to the genome (VPg) to initiate virus translation. From the yeast two-hybrid system (Y2H) and bimolecular fluorescence complementation (BiFC) assays, the TuMV-CHN2/CHN3 VPgs could not interact with BraA.eIF4E.a/c or BraA.eIF(iso)4E.c, but they could interact with BraA.eIF(iso)4E.a in B. rapa. Further analysis indicated that the amino acid substitution L186F (nt T556C) in TuMV-UK1 VPg was important for the interaction networks between the TuMV VPg and eIF(iso)4E proteins. An interaction model of the BraA. eIF(iso)4E protein with TuMV VPg was constructed to infer the effect of the significant amino acids on the interaction of TuMV VPgs-eIF(iso)4Es, particularly whether the L186F in TuMV-UK1 VPg could change the structure of the TuMV-UK1 VPg protein, which may terminate the interaction of the BraA.eIF(iso)4E and TuMV VPg protein. This study provides new insights into the interactions between plant viruses and translation initiation factors to reveal the working of key amino acids.

Keywords

References

  1. Arroyo, R., Soto, M. J., Martinez-Zapater, J. M. and Ponz, F. 1996. Impaired cell-to-cell movement of potato virus Y in pepper plants carrying the ya (pr21) resistance gene. Mol. Plant-Microbe Interact. 1996:314-318.
  2. Ayme, V., Petit-Pierre, J., Souche, S., Palloix, A. and Moury, B. 2007. Molecular dissection of the potato virus Y VPg virulence factor reveals complex adaptations to the pvr2 resistance allelic series in pepper. J. Gen. Virol. 88:1594-1601. https://doi.org/10.1099/vir.0.82702-0
  3. Ayme, V., Souche, S., Caranta, C., Jacquemond, M., Chadoeuf, J., Palloix, A. and Moury, B. 2006. Different mutations in the genome-linked protein VPg of Potato virus Y confer virulence on the pvr23 resistance in pepper. Mol. Plant-Microbe Interact. 19:557-563. https://doi.org/10.1094/MPMI-19-0557
  4. Carrington, J. C., Kasschau, K. D., Mahajan, S. K. and Schaad, M. C. 1996. Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 8:1669-1681. https://doi.org/10.1105/tpc.8.10.1669
  5. Cavatorta, J., Perez, K. W., Gray, S. M., Van Eck, J., Yeam, I. and Jahn, M. 2011. Engineering virus resistance using a modified potato gene. Plant Biotechnol. J. 9:1014-1021. https://doi.org/10.1111/j.1467-7652.2011.00622.x
  6. Contreras-Paredes, C. A., Silva-Rosales, L., Daros, J. A., Alejandri-Ramirez, N. D. and Dinkova, T. D. 2013. The absence of eukaryotic initiation factor eIF(iso)4E affects the systemic spread of a Tobacco etch virus isolate in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 26:461-470. https://doi.org/10.1094/MPMI-09-12-0225-R
  7. Dinkova, T. D., Martinez-Castilla, L. and Cruz-Espindola, M. A. 2016. The diversification of eIF4E family members in plants and their role in the plant-virus interaction. In: Evolution of the protein synthesis machinery and its regulation, eds. by G. Hernandez and R. Jagus, pp. 187-205. Springer, Cham, Switzerland.
  8. Duan, H., Richael, C. and Rommens, C. M. 2012. Overexpression of the wild potato eIF4E-1 variant Eva1 elicits Potato virus Y resistance in plants silenced for native eIF4E-1. Transgenic Res. 21:929-938. https://doi.org/10.1007/s11248-011-9576-9
  9. Gao, Z., Johansen, E., Eyers, S., Thomas, C. L., Noel Ellis, T. H. and Maule, A. J. 2004. The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J. 40:376-385. https://doi.org/10.1111/j.1365-313X.2004.02215.x
  10. German-Retana, S., Walter, J., Doublet, B., Roudet-Tavert, G., Nicaise, V., Lecampion, C., Houvenaghel, M.-C., Robaglia, C., Michon, T. and Le Gall, O. 2008. Mutational analysis of plant cap-binding protein eIF4E reveals key amino acids involved in biochemical functions and potyvirus infection. J. Virol. 82:7601-7612. https://doi.org/10.1128/JVI.00209-08
  11. Gibbs, A. and Ohshima, K. 2010. Potyviruses and the digital revolution. Annu. Rev. Phytopathol. 48:205-223. https://doi.org/10.1146/annurev-phyto-073009-114404
  12. Jenner, C. E., Nellist, C. F., Barker, G. C. and Walsh, J. A. 2010. Turnip mosaic virus (TuMV) is able to use alleles of both eIF4E and eIF(iso)4E from multiple loci of the diploid Brassica rapa. Mol. Plant-Microbe Interact. 23:1498-1505. https://doi.org/10.1094/MPMI-05-10-0104
  13. Jenner, C. E. and Walsh, J. A. 1996. Pathotypic variation in turnip mosaic virus with special reference to European isolates. Plant Pathol. 45:848-856. https://doi.org/10.1111/j.1365-3059.1996.tb02895.x
  14. Kang, B.-C., Yeam, I., Frantz, J. D., Murphy, J. F. and Jahn, M. M. 2005. The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J. 42:392-405. https://doi.org/10.1111/j.1365-313X.2005.02381.x
  15. Kanyuka, K., Druka, A., Caldwell, D. G., Tymon, A., McCallum, N., Waugh, R. and Adams, M. J. 2005. Evidence that the recessive bymovirus resistance locus rym4 in barley corresponds to the eukaryotic translation initiation factor 4E gene. Mol. Plant Pathol. 6:449-458. https://doi.org/10.1111/j.1364-3703.2005.00294.x
  16. Kim, J., Kang, W.-H., Hwang, J., Yang, H.-B., Dosun, K., Oh, C.-S. and Kang, B.-C. 2014. Transgenic Brassica rapa plants over - expressing eIF(iso)4E variants show broad - spectrum Turnip mosaic virus (TuMV) resistance. Mol Plant Pathol. 15:615-626. https://doi.org/10.1111/mpp.12120
  17. Kim, J., Kang, W.-H., Yang, H.-B., Park, S., Jang, C.-S., Yu, H.-J. and Kang, B.-C. 2013. Identification of a broad-spectrum recessive gene in Brassica rapa and molecular analysis of the eIF4E gene family to develop molecular markers. Mol. Breed. 32:385-398. https://doi.org/10.1007/s11032-013-9878-0
  18. Lellis, A. D., Kasschau, K. D., Whitham, S. A. and Carrington, J. C. 2002. Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr. Biol. 12:1046-1051. https://doi.org/10.1016/S0960-9822(02)00898-9
  19. Leonard, S., Plante, D., Wittmann, S., Daigneault, N., Fortin, M. G. and Laliberte, J. F. 2000. Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. J. Virol. 74:7730-7737. https://doi.org/10.1128/JVI.74.17.7730-7737.2000
  20. Li, G., Lv, H., Zhang, S., Zhang, S., Li, F., Zhang, H., Qian, W., Fang, Z. and Sun, R. 2019. TuMV management for brassica crops through host resistance: retrospect and prospects. Plant Pathol. 68:1035-1044. https://doi.org/10.1111/ppa.13016
  21. Li, G., Qian, W., Zhang, S., Li, F, Zhang, S., Zhang, H., Xie, L., Wu, J., Wang, X. and Sun, R. 2017. Analysis of the protein interaction of eIF(iso)4E.a/c with TuMV-C4/UK1 in Brassica rapa ssp. chinensis. Acta Hortic. Sin. 44:1299-1308 (in Chinese).
  22. Li, G., Qian, W., Zhang, S., Zhang, S., Li, F., Zhang, H., Fang, Z., Wu, J., Wang, X. and Sun, R. 2018. Variability in eukaryotic initiation factor iso4E in Brassica rapa influences interactions with the viral protein linked to the genome of Turnip mosaic virus. Sci. Rep. 8:13588. https://doi.org/10.1038/s41598-018-31739-1
  23. Li, G.-L., Qian, W., Zhang, S.-J., Zhang, S.-F., Li, F., Zhang, H., Wu, J., Wang, X.-W. and Sun, R.-F. 2016. Development of gene-based markers for the Turnip mosaic virus resistance gene retr02 in Brassica rapa. Plant Breed. 135:466-470. https://doi.org/10.1111/pbr.12372
  24. Ling, K.-S., Harris, K. R., Meyer, J. D. F., Levi, A., Guner, N., Wehner, T. C., Bendahmane, A. and Havey, M. J. 2009. Non-synonymous single nucleotide polymorphisms in the water-melon eIF4E gene are closely associated with resistance to zucchini yellow mosaic virus. Theor. Appl. Genet. 120:191-200. https://doi.org/10.1007/s00122-009-1169-0
  25. Marandel, G., Salava, J., Abbott, A., Candresse, T. and Decroocq, V. 2009. Quantitative trait loci meta-analysis of Plum pox virus resistance in apricot (Prunus armeniaca L.): new insights on the organization and the identification of genomic resistance factors. Mol. Plant Pathol. 10:347-360. https://doi.org/10.1111/j.1364-3703.2009.00535.x
  26. Mazier, M., Flamain, F., Nicolai, M., Sarnette, V. and Caranta, C. 2011. Knock-down of both eIF4E1 and eIF4E2 genes confers broad-spectrum resistance against potyviruses in tomato. PLoS ONE 6:e29595. https://doi.org/10.1371/journal.pone.0029595
  27. Michon, T., Estevez, Y., Walter, J., German-Retana, S. and Le Gall, O. 2006. The potyviral virus genome-linked protein VPg forms a ternary complex with the eukaryotic initiation factors eIF4E and eIF4G and reduces eIF4E affinity for a mRNA cap analogue. FEBS J. 273:1312-1322. https://doi.org/10.1111/j.1742-4658.2006.05156.x
  28. Naderpour, M., Lund, O. S., Larsen, R. and Johansen, E. 2010. Potyviral resistance derived from cultivars of Phaseolus vulgaris carrying bc-3 is associated with the homozygotic presence of a mutated eIF4E allele. Mol. Plant Pathol. 11:255-263. https://doi.org/10.1111/j.1364-3703.2009.00602.x
  29. Nellist, C. F., Qian, W., Jenner, C. E., Moore, J. D., Zhang, S., Wang, X., Briggs, W. H., Barker, G. C., Sun, R. and Walsh, J. A. 2014. Multiple copies of eukaryotic translation initiation factors in Brassica rapa facilitate redundancy, enabling diversification through variation in splicing and broad-spectrum virus resistance. Plant J. 77:261-268. https://doi.org/10.1111/tpj.12389
  30. Nicaise, V., German-Retana, S., Sanjuan, R., Dubrana, M.-P., Mazier, M., Maisonneuve, B., Candresse, T., Caranta, C. and LeGall, O. 2003. The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the Potyvirus Lettuce mosaic virus. Plant Physiol. 132:1272-1282. https://doi.org/10.1104/pp.102.017855
  31. Piron, F., Nicolai, M., Minoia, S., Piednoir, E., Moretti, A., Salgues, A., Zamir, D., Caranta, C. and Bendahmane, A. 2010. An induced mutation in tomato eIF4E leads to immunity to two potyviruses. PLoS ONE 5:e11313. https://doi.org/10.1371/journal.pone.0011313
  32. Provvidenti, R. 1982. A destructive disease of garden balsam caused by a strain of turnip mosaic virus. Plant Dis. 66:1076-1077. https://doi.org/10.1094/PD-66-1076
  33. Qian, W., Zhang, S., Zhang, S., Li, F., Zhang, H., Wu, J., Wang, X., Walsh, J. A. and Sun, R. 2013. Mapping and candidate-gene screening of the novel Turnip mosaic virus resistance gene retr02 in Chinese cabbage (Brassica rapa L.). Theor. Appl. Genet. 126:179-188. https://doi.org/10.1007/s00122-012-1972-x
  34. Rodriguez-Hernandez, A. M., Gosalvez, B., Sempere, R. N., Burgos, L., Aranda, M. A. and Truniger, V. 2012. Melon RNA interference (RNAi) lines silenced for Cm-eIF4E show broad virus resistance. Mol. Plant Pathol. 13:755-763. https://doi.org/10.1111/j.1364-3703.2012.00785.x
  35. Roudet-Tavert, G., Michon, T., Walter, J., Delaunay, T., Redondo, E. and Le Gall, O. 2007. Central domain of a potyvirus VPg is involved in the interaction with the host translation initiation factor eIF4E and the viral protein HcPro. J. Gen. Virol. 88:1029-1033. https://doi.org/10.1099/vir.0.82501-0
  36. Ruffel, S., Gallois, J. L., Lesage, M. L. and Caranta, C. 2005. The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Mol. Genet. Genomics 274:346-353. https://doi.org/10.1007/s00438-005-0003-x
  37. Rusholme, R. L., Higgins, E. E., Walsh, J. A. and Lydiate, D. J. 2007. Genetic control of broad-spectrum resistance to turnip mosaic virus in Brassica rapa (Chinese cabbage). J. Gen. Virol. 88:3177-3186. https://doi.org/10.1099/vir.0.83194-0
  38. Sanfacon, H. 2015. Plant translation factors and virus resistance. Viruses 7:3392-3419. https://doi.org/10.3390/v7072778
  39. Sato, M., Nakahara, K., Yoshii, M., Ishikawa, M. and Uyeda, I. 2005. Selective involvement of members of the eukaryotic initiation factor 4E family in the infection of Arabidopsis thaliana by potyviruses. FEBS Lett. 579:1167-1171. https://doi.org/10.1016/j.febslet.2004.12.086
  40. Shattuck, V. I. 1992. The biology, epidemiology and control of turnip mosaic virus. In: Horticultural reviews, Vol. 14, ed. by J. Janick, pp. 199-238. John Wiley & Sons, New York, USA.
  41. Shopan, J., Mou, H., Zhang, L., Zhang, C., Ma, W., Walsh, J. A., Hu, Z., Yang, J. and Zhang, M. 2017. Eukaryotic translation initiation factor 2B-beta (eIF2Bβ), a new class of plant virus resistance gene. Plant J. 90:929-940. https://doi.org/10.1111/tpj.13519
  42. Wang, A. and Krishnaswamy, S. 2012. Eukaryotic translation initiation factor 4E-mediated recessiveresistance to plant viruses and its utility in crop improvement. Mol. Plant Pathol. 13:795-803. https://doi.org/10.1111/j.1364-3703.2012.00791.x
  43. Wang, X., Kohalmi, S. E., Svircev, A., Wang, A., Sanfacon, H. and Tian, L. 2013. Silencing of the host factor eIF(iso)4E gene confers Plum pox virus resistance in plum. PLoS ONE 8:e50627. https://doi.org/10.1371/journal.pone.0050627
  44. Wang, X., Wang, H., Wang, J., Sun, R., Wu, J., Liu, S., Bai, Y., Mun, J. H., Bancroft, I., Cheng, F., Huang, S., Li, X., Hua, W., Wang, J., Wang, X., Freeling, M., Pires, J. C., Paterson, A. H., Chalhoub, B., Wang, B., Hayward, A., Sharpe, A. G., Park, B.-S., Weisshaar, B., Liu, B., Li, B., Liu, B., Tong, C., Song, C., Duran, C., Peng, C., Geng, C., Koh, C., Lin, C., Edwards, D., Mu, D., Shen, D., Soumpourou, E., Li, F., Fraser, F., Conant, G., Lassalle, G., King, G. J., Bonnema, G., Tang, H., Wang, H., Belcram, H., Zhou, H., Hirakawa, H., Abe, H., Guo, H., Wang, H., Jin, H., Parkin, I. A., Batley, J., Kim, J.-S., Just, J., Li, J., Xu, J., Deng, J., Kim, J. A., Li, J., Yu, J., Meng, J., Wang, J., Min, J., Poulain, J., Wang, J., Hatakeyama, K., Wu, K., Wang, L., Fang, L., Trick, M., Links, M. G., Zhao, M., Jin, M., Ramchiary, N., Drou, N., Berkman, P. J., Cai, Q., Huang, Q., Li, R., Tabata, S., Cheng, S., Zhang, S., Zhang, S., Huang, S., Sato, S., Sun, S., Kwon, S.-J., Choi, S.-R., Lee, T.- H., Fan, W., Zhao, X., Tan, X., Xu, X., Wang, Y., Qiu, Y., Yin, Y., Li, Y., Du, Y., Liao, Y., Lim, Y., Narusaka, Y., Wang, Y., Wang, Z., Li, Z., Wang, Z., Xiong, Z., Zhang, Z. and Brassica rapa Genome Sequencing Project Consortium. 2011. The genome of the mesopolyploid crop species Brassica rapa. Nat. Genet. 43:1035-1039. https://doi.org/10.1038/ng.919