Skip to main content

Advertisement

Log in

Plant-derived ribosome-inactivating proteins involved in defense against plant viruses

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Plant viruses are the most serious pathogens causing severe damage to crops worldwide. A variety of conventional strategies are currently being employed to control the infection and minimize the pathogenic effects of plant viruses. Developing induced resistance in plants against viruses is an effective approach. The resistance-inducing antiviral proteins from non-host plants could be utilized against a variety of viruses. It is known that plants produce ribosome inactivating proteins (RIPs) which confer resistance against different virus infections. These proteins, when exogenously applied on leaves, are easily absorbed into the damaged local tissue, and sometimes its induction translocated into the whole plant. Once the virus is inoculated, these proteins become responsible for inhibiting the virus multiplication in host plants. In this review, the involvement of RIPs of plant origin in defense against plant viruses is well summarized, and the mechanism of antiviral action is discussed. The transgenic approach utilizing RIPs for antiviral effects has also been emphasized on. This study provides in-depth insights about the antiviral activity of different RIPs and their potential role in reducing the effect of virus infections in plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Balasaraswathi, R., Sadasivam, S., Ward, M., & Walker, J. M. (1998). An antiviral protein from Bougainvillea spectabilis roots; purification and characterisation. Phytochemistry, 47, 1561–1565.

    Article  CAS  PubMed  Google Scholar 

  • Balasubrahmanyam, A., Baranwal, V. K., Lodha, M. L., Varma, A., & Kapoor, H. C. (2000). Purification and properties of growth stage dependent antiviral proteins from the leaves of Celosia cristata. Plant Science, 154, 13–21.

    Article  CAS  PubMed  Google Scholar 

  • Baranwal, V. K., & Verma, H. N. (1992). Localized resistance against virus infection by leaf extract of Celosia cristata. Plant Pathology, 41, 633–638.

    Article  Google Scholar 

  • Baranwal, V. K., Tumer, N. E., & Kapoor, H. C. (2002). Depurination of ribosomal RNA and inhibition of viral RNA translation by an antiviral protein of Celosia cristata. Indian Journal of Experimental Biology, 40, 1195–1197.

    CAS  PubMed  Google Scholar 

  • Barbieri, L., Aron, G. M., Irvin, J. D., & Stirpe, F. (1982). Purification and partial characterization of another form of the antiviral protein from the seeds of Phytolacca americana L. (pokeweed). The Biochemical Journal, 203, 55–59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbieri, L., Gorini, P., Valbonesi, P., Castiglioni, P., & Stirpe, F. (1994). Unexpected activity of saporins. Nature, 372, 624.

    Article  CAS  PubMed  Google Scholar 

  • Barbieri, L., Valbonesi, P., Bonora, E., Gorini, P., Bolognesi, A., & Stirpe, F. (1997). Polynucleotide: Adenosine glycosidase activity of ribosome-inactivating proteins: Effect on DNA, RNA and poly(A). Nucleic Acids Research, 25, 518–522.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Begam, M., Narwal, S., Roy, S., Kumar, S., Lodha, M. L., & Kapoor, H. C. (2006). An antiviral protein having deoxyribonuclease and ribonuclease activity from leaves of the post-flowering stage of Celosia cristata. Biochemistry (moscow), 71, S44–S48.

    Article  CAS  Google Scholar 

  • Bhatia, S., Kapoor, H. C., & Lodha, M. L. (2004). Modification of antioxidant status of host cell in response to Bougainvillea antiviral proteins. Journal of Plant Biochemistry and Biotechnology, 13, 113–118.

    Article  CAS  Google Scholar 

  • Bhatia, S., & Lodha, M. L. (2005). RNase and DNase activities of antiviral proteins from leaves of Bougainvillea xbuttiana. Indian Journal of Biochemistry & Biophysics, 42, 152–155.

    CAS  Google Scholar 

  • Bolognesi, A., Polito, L., Olivieri, F., Valbonesi, P., Barbieri, L., Battelli, M. G., Carusi, M. V., Benvenuto, E., Del Vecchio Blanco, F., Di Maro, A., Parente, A., Di Loreto, M., & Stirpe, F. (1997). New ribosome-inactivating proteins with polynucleotide:Adenosine glycosidase and antiviral activities from Basella rubra L. and Bougainvillea spectabilis Willd. Planta, 203, 422–429.

    Article  CAS  PubMed  Google Scholar 

  • Bolognesi, A., Bortolotti, M., Maiello, S., Battelli, M. G., & Polito, L. (2016). Ribosome-inactivating proteins from plants: A historical overview. Molecules, 21, 1627.

    Article  PubMed Central  Google Scholar 

  • Bulgari, D., Landi, N., Ragucci, S., Faoro, F., & Di Maro, A. (2020). Antiviral activity of PD-L1 and PD-L4, type 1 ribosome inactivating proteins from leaves of Phytolacca dioica L. in the pathosystem Phaseolus vulgaris–tobacco necrosis virus (TNV). Toxins, 12, 524.

  • Cao, B., Lei, J., Chen, G., Cao, P., Liu, X., Chen, Q., & Wei, X. (2011). Testing of disease-resistance of pokeweed antiviral protein gene (PacPAP) in transgenic cucumber (Cucumis sativus). African Journal of Biotechnology, 10, 6883–6890.

    CAS  Google Scholar 

  • Carzaniga, R., Sinclair, L., Fordham-Skelton, A. P., Harris, N., & Croy, R. R. D. (1994). Cellular and subcellular distribution of saporins, type-1 ribosome-inactivating proteins, in soapwort (Saponaria officinalis L.). Planta, 194, 461–470.

    Article  CAS  Google Scholar 

  • Chen, Z., White, R. F., Antoniw, J. F., & Lin, Q. (1991). Effect of pokeweed antiviral protein (PAP) on the infection of plant viruses. Plant Pathology, 40, 612–620.

    Article  Google Scholar 

  • Chen, Z., Antoniw, J. F., & White, R. F. (1993). A possible mechanism for the antiviral activity of pokeweed antiviral protein. Physiological and Molecular Plant Pathology, 42, 249–258.

    Article  CAS  Google Scholar 

  • Chen, Y., Peumans, W. J., & Van Damme, E. J. M. (2002). The Sambucus nigra type-2 ribosome-inactivating protein SNA-I’ exhibits in planta antiviral activity in transgenic tobacco. FEBS Letters, 516, 27–30.

    Article  CAS  PubMed  Google Scholar 

  • Chen, G. J., Shi, L., Lei, J. J., Cao, B. H., & Zeng, G. P. (2008). Cloning of pokeweed antiviral protein gene from Phytolacca acinosa and its transfer to pepper (Capsicum annuum L.). Acta Horticulturae Sinica, 35, 847–852.

    CAS  Google Scholar 

  • Cho, H. J., Lee, S. J., Kim, S., & Kim, B. D. (2000a). Isolation and characterization of cDNAs encoding ribosome inactivating protein from Dianthus sinensis L. Molecules and Cells, 10, 135–141.

    CAS  PubMed  Google Scholar 

  • Cho, K. J., Lee, S. M., Kim, Y. T., & Hwang, Y. S. (2000b). Purification and characterization of an antiviral ribosome-inactivating protein from Chenopodium album L. Journal of Applied Biological Chemistry, 43, 125–130.

    CAS  Google Scholar 

  • Choudhary, N., Kapoor, H. C., & Lodha, M. L. (2008a). Cloning and expression of antiviral/ribosome-inactivating protein from Bougainvillea xbuttiana. Journal of Biosciences, 33, 91–101.

    Article  CAS  PubMed  Google Scholar 

  • Choudhary, N. L., Yadav, O. P., & Lodha, M. L. (2008b). Ribonuclease, deoxyribonuclease, and antiviral activity of Escherichia coli-expressed Bougainvillea xbuttiana antiviral protein. Biochemistry, 73, 273–277.

    CAS  PubMed  Google Scholar 

  • Choudhary, N., Lodha, M. L., & Baranwal, V. K. (2020). The role of enzymatic activities of antiviral proteins from plants for action against plant pathogens. 3 Biotech, 10, 505.

  • Cillo, F., & Palukaitis, P. (2014). Transgenic resistance. Advances in Virus Research, 90, 35–146.

    Article  CAS  PubMed  Google Scholar 

  • Citores, L., Iglesias, R., & Ferreras, J. M. (2021). Antiviral activity of ribosome-inactivating proteins. Toxins, 13, 80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corrado, G., Scarpetta, M., Alioto, D., Di Maro, A., Polito, L., Parente, A., & Rao, R. (2008). Inducible antiviral activity and rapid production of the ribosome-inactivating protein I from Phytolacca heterotepala in tobacco. Plant Science, 174, 467–474.

    Article  CAS  Google Scholar 

  • Dasgupta, I., Malathi, V., & Mukherjee, S. (2003). Genetic engineering for virus resistance. Current Science, 84, 341–354.

    CAS  Google Scholar 

  • de Virgilio, M., Lombardi, A., Caliandro, R., & Fabbrini, M. S. (2010). Ribosome inactivating proteins: From plant defense to tumor attack. Toxins, 2, 2699–2737.

    Article  PubMed  PubMed Central  Google Scholar 

  • Desmyter, S., Vandenbussche, F., Hao, Q., Proost, P., Peumans, W. J., & Van Damme, E. J. M. (2003). Type-1 ribosome-inactivating protein from iris bulbs: A useful agronomic tool to engineer virus resistance? Plant Molecular Biology, 51, 567–576.

    Article  CAS  PubMed  Google Scholar 

  • Di Maro, A., Citores, L., Russo, R., Iglesias, R., & Ferreras, J. M. (2014). Sequence comparison and phylogenetic analysis by the maximum likelihood method of ribosome-inactivating proteins from angiosperms. Plant Molecular Biology, 85, 575–588.

    Article  PubMed  Google Scholar 

  • Di, R., & Tumer, N. E. (2005). Expression of a truncated form of ribosomal protein L3 confers resistance to pokeweed antiviral protein and the Fusarium mycotoxin deoxynivalenol. Molecular Plant-Microbe Interactions, 18, 762–770.

    Article  CAS  PubMed  Google Scholar 

  • Di, R., & Tumer, N. E. (2015). Pokeweed antiviral protein: Its cytotoxicity mechanism and applications in plant disease resistance. Toxins, 7, 755–772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Domashevskiy, A. V., & Cheng, S. Y. (2015). Thermodynamic analysis of binding and enzymatic properties of pokeweed antiviral protein (PAP) toward tobacco etch virus (TEV) RNA. Journal of Nature and Science, 1, e82.

  • Domashevskiy, A. V., Williams, S., Kluge, C., & Cheng, S. Y. (2017). Plant translation initiation complex eIFiso4F directs pokeweed antiviral protein to selectively depurinate uncapped tobacco etch virus RNA. Biochemistry, 56, 5980–5990.

    Article  CAS  PubMed  Google Scholar 

  • Dutt, S., Balasubrahmanyam, A., & Lodha, M. L. (2000). Purification and partial characterization of antiviral proteins from Chenopodium album L. leaves. Journal of Plant Physiology, 156, 808–810.

    Article  CAS  Google Scholar 

  • Dutt, S., Narwal, S., Kapoor, H. C., & Lodha, M. L. (2003). Isolation and characterization of two protein isoforms with antiviral activity from Chenopodium album L leaves. Journal of Plant Biochemistry and Biotechnology, 12, 117–122.

    Article  CAS  Google Scholar 

  • Dutt, S., Yadav, O. P., Kapoor, H. C., & Lodha, M. L. (2004). Possible mechanism of action of antiviral proteins from the leaves of Chenopodium album L. Indian Journal of Biochemistry & Biophysics, 41, 29–33.

    CAS  Google Scholar 

  • Endo, Y., Tsurugi, K., & Lambert, J. M. (1988). The site of action of six different ribosome-inactivating proteins from plants on eukaryotic ribosomes: The RNA N-glycosidase activity of the proteins. Biochemical and Biophysical Research Communications, 150, 1032–1036.

    Article  CAS  PubMed  Google Scholar 

  • Fabbrini, M. S., Katayama, M., Nakase, I., & Vago, R. (2017). Plant ribosome-inactivating proteins: Progesses, challenges and biotechnological applications (and a few digressions). Toxins, 9, 314.

    Article  PubMed Central  Google Scholar 

  • Fu, D. L., Wang, L. L., Zhang, H. Y., & Chen, Z. H. (2000). Introduction of PAP cDNA into potato by the laser microbeam puncture techniques. Acta Photonica Sinica, 29, 970–974.

    Google Scholar 

  • Gandhi, R., Manzoor, M., & Hudak, K. A. (2008). Depurination of brome mosaic virus RNA3 in vivo results in translation-dependent accelerated degradation of the viral RNA. The Journal of Biological Chemistry, 283, 32218–32228.

    Article  CAS  PubMed  Google Scholar 

  • Gholizadeh, A., Kumar, M., Balasubrahmanyam, A., Sharma, S., Narwal, S., Lodha, M., & Kapoor, H. (2004). Antioxidant activity of antiviral proteins from Celosia cristata. Journal of Plant Biochemistry and Biotechnology, 13, 13–18.

    Article  CAS  Google Scholar 

  • Gholizadeh, A., & Pourrahim, R. (2017). Identification and differential biophysical characterization of antiviral potentials from different Celosia plants. Plant Cell Biotechnology and Molecular Biology, 18, 527–534.

    Google Scholar 

  • Gholizadeh, A. (2019). Purification of a ribosome-inactivating protein with antioxidation and root developer potencies from Celosia plumosa. Physiology and Molecular Biology of Plants, 25, 243–251.

    Article  CAS  PubMed  Google Scholar 

  • Girbés, T., de Torre, C., Iglesias, R., Ferreras, J. M., & Méndez, E. (1996). RIP for viruses. Nature, 379, 777–778.

    Article  Google Scholar 

  • Girbés, T., Ferreras, J. M., Arias, F. J., & Stirpe, F. (2004). Description, distribution, activity and phylogenetic relationship of ribosome-inactivating proteins in plants, fungi and bacteria. Mini-Reviews in Medicinal Chemistry, 4, 461–476.

    Article  PubMed  Google Scholar 

  • Güller, A., Sipahioğlu, H. M., Usta, M., & Durak, E. D. (2018). Antiviral and antifungal activity of biologically active recombinant bouganin protein from Bougainvillea spectabilis willd. Journal of Agricultural Sciences, 24, 227–237.

    Google Scholar 

  • Hao, Q., Van Damme, E. J. M., Hause, B., Barre, A., Chen, Y., Rouge, P., & Peumans, W. J. (2001). Iris bulbs express type 1 and type 2 ribosome- inactivating proteins with unusual properties. Plant Physiology, 125, 866–876.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartley, M. R., & Lord, J. M. (2004). Genetics of ribosome-inactivating proteins. Mini-Reviews in Medicinal Chemistry, 4, 487–492.

    Article  CAS  PubMed  Google Scholar 

  • Hiramatsu, A., Kobayashi, N., & Osawa, N. (1987). Properties of two inhibitors of plant virus infection from fruiting bodies of Lentinus edodes and from leaves of Yucca recurvifolia salisb. Agricultural and Biological Chemistry, 51, 897–904.

    CAS  Google Scholar 

  • Hong, Y., Saunders, K., Hartley, M. R., & Stanley, J. (1996). Resistance to geminivirus infection by virus-induced expression of dianthin in transgenic plants. Virology, 220, 119–127.

    Article  CAS  PubMed  Google Scholar 

  • Hornung, E., Wajant, H., Jeske, H., & Mundry, K. W. (1996). Cloning of a cDNA encoding a new ribosome-inactivating protein from Beta vulgaris vulgaris (mangold). Gene, 170, 233–236.

    Article  CAS  PubMed  Google Scholar 

  • Horsch, R. B., Fry, J. E., Hoffmann, N. L., Eichholtz, D., Rogers, S. G., & Fraley, R. T. (1985). A simple and general method for transferring genes into plants. Science, 227, 1229–1231.

    Article  CAS  Google Scholar 

  • Huang, M., Hou, P., Wei, Q., Xu, Y., & Chen, F. (2008). A ribosome-inactivating protein (curcin 2) induced from Jatropha curcas can reduce viral and fungal infection in transgenic tobacco. Plant Growth Regulation, 54, 115–123.

    Article  CAS  Google Scholar 

  • Hudak, K. A., Dinman, J. D., & Tumer, N. E. (1999). Pokeweed antiviral protein accesses ribosomes by binding to L3. The Journal of Biological Chemistry, 274, 3859–3864.

    Article  CAS  PubMed  Google Scholar 

  • Hudak, K. A., Wang, P., & Tumer, N. E. (2000). A novel mechanism for inhibition of translation by pokeweed antiviral protein: Depurination of the capped RNA template. RNA, 6, 369–380.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iglesias, R., Pérez, Y., de Torre, C., Ferreras, J. M., Antolín, P., Jiménez, P., Rojo, M. A., Méndez, E., & Girbés, T. (2005). Molecular characterization and systemic induction of single-chain ribosome-inactivating proteins (RIPs) in sugar beet (Beta vulgaris) leaves. Journal of Experimental Botany, 56, 1675–1684.

    Article  CAS  PubMed  Google Scholar 

  • Iglesias, R., Pérez, Y., Citores, L., Ferreras, J. M., Méndez, E., & Girbés, T. (2008). Elicitor-dependent expression of the ribosome-inactivating protein beetin is developmentally regulated. Journal of Experimental Botany, 59, 1215–1223.

    Article  CAS  PubMed  Google Scholar 

  • Iglesias, R., Citores, L., Ragucci, S., Russo, R., Di Maro, A., & Ferreras, J. M. (2016). Biological and antipathogenic activities of ribosome-inactivating proteins from Phytolacca dioica L. Biochimica Et Biophysica Acta, 1860, 1256–1264.

    Article  CAS  PubMed  Google Scholar 

  • Irvin, J. D., Kelly, T., & Robertus, J. D. (1980). Purification and properties of a second antiviral protein from Phytolacca americana which inactivates eukaryotic ribosomes. Archives of Biochemistry and Biophysics, 200, 418–425.

    Article  CAS  PubMed  Google Scholar 

  • Ito, Y., Seki, I., Tanifuji, S., & Hiramatsu, A. (1993). Inhibition of protein synthesis by antiviral protein from Yucca recurvifolia leaves. Bioscience, Biotechnology, and Biochemistry, 57, 518–519.

    Article  CAS  Google Scholar 

  • Jiang, G. Y., Weng, M. L., Jin, D. M., & Wang, B. (1998). Characteristics of TCS transgenic tomato. Acta Horticulturae Sinica, 25, 395–396.

    Google Scholar 

  • Jiang, G. Y., Jin, D. M., Weng, M. L., Guo, B. T., & Wang, B. (1999). Transformation and expression of trichosanthin gene in tomato. Journal of Integrative Plant Biology, 41, 334–336.

    CAS  Google Scholar 

  • Kammen, A. V., Noordam, D., & Thung, T. H. (1961). The mechanism of inhibition of infection with tobacco mosaic virus by an inhibitor from carnation sap. Virology, 14, 100–108.

    Article  Google Scholar 

  • Karran, R. A., & Hudak, K. A. (2008). Depurination within the intergenic region of brome mosaic virus RNA3 inhibits viral replication in vitro and in vivo. Nucleic Acids Research, 36, 7230–7239.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karran, R. A., & Hudak, K. A. (2011). Depurination of brome mosaic virus RNA3 inhibits its packaging into virus particles. Nucleic Acids Research, 39, 7209–7222.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, Y. S., Park, S. C., Oh, S. K., Lee, H., Cho, J. W., & Chung, C. H. (1999a). Antiviral proteins, amarandin 1 and 2, from Amaranthus viridis, DNAs encoding therefrom. United States Patent No. 6001986-A.

  • Kim, Y. S., Park, S. C., Oh, S. K., Lee, H., Cho, J. W., & Chung, C.H. (1999b). DNA encoding amarandin-S ribosome inactivating protein of Amaranthus viridis. United States Patent No. 5977335-A.

  • Krishnan, R., McDonald, K. A., Dandekar, A. M., Jackman, A. P., & Falk, B. (2002). Expression of recombinant trichosanthin, a ribosome-inactivating protein, in transgenic tobacco. Journal of Biotechnology, 97, 69–88.

    Article  CAS  PubMed  Google Scholar 

  • Kubo, S., Ikeda, T., Imaizumi, S., Takanami, Y., & Mikami, Y. (1990). A potent plant virus inhibitor found in Mirabilis jalapa L. Annals of Phytopathological Society of Japan, 56, 481–487.

    Article  Google Scholar 

  • Kumar, M. A., Timm, D. E., Neet, K. E., Owen, W. G., Peumans, W. J., & Rao, A. G. (1993). Characterization of the lectin from the bulbs of Eranthis hyemalis (winter aconite) as an inhibitor of protein synthesis. The Journal of Biological Chemistry, 268, 25176–25183.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, D., Verma, H. N., Tuteja, N., & Tewari, K. K. (1997). Cloning and characterisation of a gene encoding an antiviral protein from Clerodendrum aculeatum L. Plant Molecular Biology, 33, 745–751.

    Article  CAS  PubMed  Google Scholar 

  • Kwon, S. Y., An, C. S., Liu, J. R., & Paek, K. H. (1997). A ribosome-inactivating protein from Amaranthus viridis. Bioscience, Biotechnology, and Biochemistry, 61, 1613–1614.

    Article  CAS  PubMed  Google Scholar 

  • Kwon, S. Y., An, C. S., Liu, J. R., Kwak, S. S., Lee, H. S., Kim, J. K., & Paek, K. H. (2000). Molecular cloning of a cDNA encoding ribosome inactivating protein from Amaranthus viridis and its expression in E. coli. Molecules and Cells, 10, 8–12.

    Article  CAS  PubMed  Google Scholar 

  • Lam, Y. H., Wong, Y. S., Wang, B., Wong, R. N. S., Yeung, H. W., & Shaw, P. C. (1996). Use of trichosanthin to reduce infection by turnip mosaic virus. Plant Science, 114, 111–117.

    Article  CAS  Google Scholar 

  • Lee, S., Cho, K., Kim, Y., Park, H., Kim, S., Hwang, Y., & Kim, D. (1999). Antiviral activity of a type 1 ribosome-inactivating protein from Chenopodium album L. Journal of Applied Biological Chemistry, 42, 161–165.

    CAS  Google Scholar 

  • Li, Y., Jia, Y., Zhang, Z., Chen, X., He, H., Fang, R., & Hao, X. (2007). Purification and characterization of a new ribosome inactivating protein from cinchonaglycoside C-treated tobacco leaves. Journal of Integrative Plant Biology, 49, 1327–1333.

    Article  CAS  Google Scholar 

  • Li, L., Li, Y., Chen, D., Feng, H., & Wang, X. (2013). Improved resistance to cucumber mosaic virus in Petunia transformed with non-cytotoxic pokeweed antiviral protein gene. Journal of Phytopathology, 161, 239–245.

    Article  CAS  Google Scholar 

  • Lodge, J. K., Kaniewski, W. K., & Tumer, N. E. (1993). Broad-spectrum virus resistance in transgenic plants expressing pokeweed antiviral protein. Proceedings of the National Academy of Sciences of the United States of America, 90, 7089–7093.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lodha, M. L., Agarwal, S., Biswas, K., Vasudev, S., & Dubey, S. C. (2010). Antimicrobial activity of native and recombinant antiviral proteins from Bougainvillea xbuttiana leaves against plant pathogenic fungi and viruses. Indian Journal of Agricultural Biochemistry, 23, 83–90.

    CAS  Google Scholar 

  • Mansouri, S., Nourollahzadeh, E., & Hudak, K. A. (2006). Pokeweed antiviral protein depurinates the sarcin/ricin loop of the rRNA prior to binding of aminoacyl-tRNA to the ribosomal A-site. RNA, 12, 1683–1692.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moon, Y. H., Jeon, H. S., Choi, K. W., & Lee, J. S. (1994). Development of virus-resistant potato by expression of Phytolacca antiviral protein. Molecules and Cells, 4, 183–188.

    CAS  Google Scholar 

  • Moon, Y. H., Song, S. K., Choi, K. W., & Lee, J. S. (1997). Expression of a cDNA encoding Phytolacca insularis antiviral protein confers virus resistance on transgenic potato plants. Molecules and Cells, 7, 807–815.

    CAS  PubMed  Google Scholar 

  • Musidlak, O., Nawrot, R., & Goździcka-Józefiak, A. (2017). Which plant proteins are involved in antiviral defense? review on in vivo and in vitro activities of selected plant proteins against viruses. International Journal of Molecular Sciences, 18, 2300.

    Article  PubMed Central  Google Scholar 

  • Narwal, S., Balasubrahmanyam, A., Lodha, M. L., & Kapoor, H. C. (2001a). Purification and properties of antiviral proteins from the leaves of Bougainvillea xbuttiana. Indian Journal of Biochemistry & Biophysics, 38, 342–347.

    CAS  Google Scholar 

  • Narwal, S., Balasubrahmanyam, A., Sadhna, P., Kapoor, H., & Lodha, M. L. (2001b). A systemic resistance inducing antiviral protein with N-glycosidase activity from Bougainvillea xbuttiana leaves. Indian Journal of Experimental Biology, 39, 600–603.

    CAS  PubMed  Google Scholar 

  • Ng, T. B., Wong, J. H., & Wang, H. (2010). Recent progress in research on ribosome inactivating proteins. Current Protein & Peptide Science, 11, 37–53.

    Article  CAS  Google Scholar 

  • Nielsen, K., & Boston, R. S. (2001). Ribosome-inactivating proteins: A plant perspective. Annual Review of Plant Physiology and Plant Molecular Biology, 52, 785–816.

    Article  CAS  PubMed  Google Scholar 

  • Olivieri, F., Prasad, V., Valbonesi, P., Srivastava, S., Ghosal-Chowdhury, P., Barbieri, L., Bolognesi, A., & Stirpe, F. (1996). A systemic antiviral resistance-inducing protein isolated from Clerodendrum inerme Gaertn. is a polynucleotide:Adenosine glycosidase (ribosome-inactivating protein). FEBS Letters, 396, 132–134.

    Article  CAS  PubMed  Google Scholar 

  • Osawa, N., & Hiramatsu, A. (1987). Purification and chemical properties of an inhibitor of plant virus infection from leaves of Yucca recurvifolia salisb. Agricultural and Biological Chemistry, 51, 891–896.

    CAS  Google Scholar 

  • Parente, A., Conforto, B., Di Maro, A., Chambery, A., De Luca, P., Bolognesi, A., Iriti, M., & Faoro, F. (2008). Type 1 ribosome-inactivating proteins from Phytolacca dioica L. leaves: Differential seasonal and age expression, and cellular localization. Planta, 228, 963–975.

    Article  CAS  PubMed  Google Scholar 

  • Parikh, B. A., Coetzer, C., & Tumer, N. E. (2002). Pokeweed antiviral protein regulates the stability of its own mRNA by a mechanism that requires depurination but can be separated from depurination of the alpha-sarcin/ricin loop of rRNA. The Journal of Biological Chemistry, 277, 41428–41437.

    Article  CAS  PubMed  Google Scholar 

  • Park, S. W., Vepachedu, R., Sharma, N., & Vivanco, J. M. (2004). Ribosome-inactivating proteins in plant biology. Planta, 219, 1093–1096.

    Article  CAS  PubMed  Google Scholar 

  • Peumans, W. J., Hao, Q., & Van Damme, E. J. M. (2001). Ribosome-inactivating proteins from plants: More than RNA N-glycosidases? FASEB Journal, 15, 1493–1506.

    Article  CAS  PubMed  Google Scholar 

  • Picard, D., Kao, C. C., & Hudak, K. A. (2005). Pokeweed antiviral protein inhibits brome mosaic virus replication in plant cells. The Journal of Biological Chemistry, 280, 20069–20075.

    Article  CAS  PubMed  Google Scholar 

  • Prasad, V., Srivastava, S., & Varsha, & Verma, H. N. (1995). Two basic proteins isolated from Clerodendrum inerme Gaertn. are inducers of systemic antiviral resistance in susceptible plants. Plant Science, 110, 73–82.

    Article  CAS  Google Scholar 

  • Prasad, V., Mishra, S. K., Srivastava, S., & Srivastava, A. (2014). A virus inhibitory protein isolated from Cyamopsis tetragonoloba (L.) Taub. upon induction of systemic antiviral resistance shares partial amino acid sequence homology with a lectin. Plant Cell Reports, 33, 1467–1478.

    Article  CAS  PubMed  Google Scholar 

  • Prestle, J., Schönfelder, M., Adam, G., & Mundry, K. W. (1992). Type 1 ribosome-inactivating proteins depurinate plant 25S rRNA without species specificity. Nucleic Acids Research, 20, 3179–3182.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin, W., Ming-Xing, H., Ying, X., Xin-Shen, Z., & Fang, C. (2005). Expression of a ribosome inactivating protein (curcin 2) in Jatropha curcas is induced by stress. Journal of Biosciences, 30, 351–357.

    Article  PubMed  Google Scholar 

  • Ragetli, H. W. J., & Weixtraub, M. (1962). Purification and characteristics of a virus inhibitor from Dianthus caryophyllus L. 1 purification and activity. Virology, 18, 232–240.

    Article  CAS  PubMed  Google Scholar 

  • Rajamohan, F., Venkatachalam, T. K., Irvin, J. D., & Uckun, F. M. (1999). Pokeweed antiviral protein isoforms PAP-I, PAP-II, and PAP-III depurinate RNA of human immunodeficiency virus (HIV)-1. Biochemical and Biophysical Research Communications, 260, 453–458.

    Article  CAS  PubMed  Google Scholar 

  • Ready, M., Brown, D. T., & Robertus, J. D. (1986). Extracellular localization of pokeweed antiviral protein. Proceedings of the National Academy of Sciences of the United States of America, 83, 5053–5056.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roy, S., Sadhana, P., Begum, M., Kumar, S., Lodha, M. L., & Kapoor, H. C. (2006). Purification, characterization and cloning of antiviral/ribosome inactivating protein from Amaranthus tricolor leaves. Phytochemistry, 67, 1865–1873.

    Article  CAS  PubMed  Google Scholar 

  • Ruan, X. L., Liu, L. F., & Li, H. (2007). Transgenic tobacco plants with ribosome inactivating protein gene cassin from Cassia occidentalis and their resistance to tobacco mosaic virus. Journal of Plant Physiology and Molecular Biology, 33, 517–523.

    CAS  PubMed  Google Scholar 

  • Rustgi, S., Pollmann, S., Buhr, F., Springer, A., Reinbothe, C., von Wettstein, D., & Reinbothe, S. (2014). JIP60-mediated, jasmonate- and senescence-induced molecular switch in translation toward stress and defense protein synthesis. Proceedings of the National Academy of Sciences of the United States of America, 111, 14181–14186.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schrot, J., Weng, A., & Melzig, M. F. (2015). Ribosome-inactivating and related proteins. Toxins, 7, 1556–1615.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi, W. W., Mak, A. N., Wong, K. B., & Shaw, P. C. (2016). Structures and ribosomal interaction of ribosome-inactivating proteins. Molecules, 21, 1588.

    Article  PubMed Central  Google Scholar 

  • Singh, S., Awasthi, L. P., & Singh, R. K. (2011). Induction of systemic resistance through antiviral agents of plant origin against papaya ring spot disease (Carica papaya L.). Archives of Phytopathology and Plant Protection, 44, 1676–1682.

    Article  Google Scholar 

  • Sipahioglu, H. M., Kaya, I., Usta, M., Ünal, M., Ozcan, D., Özer, M., Güller, A., & Pallás, V. (2017). Pokeweed (Phytolacca americana L.) antiviral protein inhibits zucchini yellow mosaic virus infection in a dose-dependent manner in squash plants. Turkish Journal of Agriculture and Forestry, 41, 256–262.

    Article  CAS  Google Scholar 

  • Smirnov, S., Shulaev, V., & Tumer, N. E. (1997). Expression of pokeweed antiviral protein in transgenic plants induced virus resistance in grafted wild-type plants independently of salicylic acid accumulation and pathogenesis-related protein synthesis. Plant Physiology, 114, 1113–1121.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smookler, M. M. (1971). Properties of inhibitors of plant virus infection occurring in the leaves of species in the Chenopodiales. Annals of Applied Biology, 69, 157–168.

    Article  Google Scholar 

  • Song, S. K., Choi, Y., Moon, Y. H., Kim, S. G., Choi, Y. D., & Lee, J. S. (2000). Systemic induction of a Phytolacca insularis antiviral protein gene by mechanical wounding, jasmonic acid, and abscisic acid. Plant Molecular Biology, 43, 439–450.

    Article  CAS  PubMed  Google Scholar 

  • Srivastava, A., Trivedi, S., Krishna, S. K., Verma, H. N., & Prasad, V. (2009). Suppression of papaya ringspot virus infection in Carica papaya with CAP-34, a systemic antiviral resistance inducing protein from Clerodendrum aculeatum. European Journal of Plant Pathology, 123, 241–246.

    Article  CAS  Google Scholar 

  • Srivastava, S., Verma, H. N., Srivastava, A., & Prasad, V. (2015a). BDP-30, a systemic resistance inducer from Boerhaavia diffusa L., suppresses TMV infection, and displays homology with ribosome-inactivating proteins. Journal of Biosciences, 40, 125–135.

    Article  CAS  PubMed  Google Scholar 

  • Srivastava, A., Srivastava, S., & Prasad, V. (2015b). Systemic antiviral resistance induced in papaya by CAP-34, a resistance inducing protein from Clerodendrum aculeatum, is associated with a proteinaceous virus inhibitory activity. Journal of Plant Pathology, 97, 45–54.

    Google Scholar 

  • Stirpe, F., Williams, D. G., Onyon, L. J., Legg, R. F., & Stevens, W. A. (1981). Dianthins, ribosome-damaging proteins with anti-viral properties from Dianthus caryophyllus L. (carnation). The Biochemical Journal, 195, 399–405.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stirpe, F. (2004). Ribosome-inactivating proteins. Toxicon, 44, 371–383.

    Article  CAS  PubMed  Google Scholar 

  • Stirpe, F. (2013). Ribosome-inactivating proteins: From toxins to useful proteins. Toxicon, 67, 12–16.

    Article  CAS  PubMed  Google Scholar 

  • Stirpe, F., & Battelli, M. G. (2006). Ribosome-inactivating proteins: Progress and problems. Cellular and Molecular Life Sciences, 63, 1850–1866.

    Article  CAS  PubMed  Google Scholar 

  • Straub, P., Adam, G., & Mundry, K. W. (1986). Isolation and characterization of a virus inhibitor from spinach (Spinacia oleracea L.). Journal of Phytopathology, 115, 357–367.

    Article  CAS  Google Scholar 

  • Takanami, Y., Kuwata, S., Ikeda, T., & Kubo, S. (1990). Purification and characterization of the anti-plant viral protein from Mirabilis jalapa L. Annals of Phytopathological Society of Japan, 56, 488–494.

    Article  CAS  Google Scholar 

  • Taylor, B. E., & Irvin, D. (1990). Depurination of plant ribosomes by pokeweed antiviral protein. FEBS Letters, 273, 144–146.

    Article  CAS  PubMed  Google Scholar 

  • Taylor, S., Massiah, A., Lomonossoff, G., Roberts, L. M., Lord, J. M., & Hartley, M. (1994). Correlation between the activities of five ribosome-inactivating proteins in depurination of tobacco ribosomes and inhibition of tobacco mosaic virus infection. The Plant Journal, 5, 827–835.

    Article  CAS  PubMed  Google Scholar 

  • Torky, Z. A. (2012). Isolation and characterization of antiviral protein from Salsola longifolia leaves expressing polynucleotide adenosine glycoside activity. The Online Journal of Science and Technology, 2, 52–58.

    Google Scholar 

  • Tumer, N. E., Hwang, D. J., & Bonness, M. (1997). C-terminal deletion mutant of pokeweed antiviral protein inhibits viral infection but does not depurinate host ribosomes. Proceedings of the National Academy of Sciences of the United States of America, 94, 3866–3871.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Damme, E. J. M., Barre, A., Barbieri, L., Valbonesi, P., Rouge, P., Van Leuven, F., Stirpe, F., & Peumans, W. J. (1997). Type 1 ribosome-inactivating proteins are the most abundant proteins in iris (Iris hollandica var. Professor Blaauw) bulbs: Characterization and molecular cloning. The Biochemical Journal, 324, 963–970.

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Damme, E. J. M., Hao, Q., Chen, Y., Barre, A., Vandenbussche, E., Desmyster, S., Rouse, P., & Peuman, W. J. (2001). Ribosome-inactivating proteins: A family of plant proteins that do more than inactivate ribosome. Critical Reviews in Plant Sciences, 20, 395–465.

    Article  Google Scholar 

  • Vandenbussche, F., Desmyter, S., Ciani, M., Proost, P., Peumans, W. J., & Van Damme, E. J. M. (2004a). Analysis of the in planta antiviral activity of elderberry ribosome-inactivating proteins. European Journal of Biochemistry, 271, 1508–1515.

    Article  CAS  PubMed  Google Scholar 

  • Vandenbussche, F., Peumans, W. J., Desmyter, S., Proost, P., Ciani, M., & Van Damme, E. J. M. (2004b). The type-1 and type-2 ribosome-inactivating proteins from Iris confer transgenic tobacco plants local but not systemic protection against viruses. Planta, 220, 211–221.

    Article  CAS  PubMed  Google Scholar 

  • Vepachedu, R., Bais, H. P., & Vivanco, J. M. (2003). Molecular characterization and post-transcriptional regulation of ME1, a type-I ribosome-inactivating protein from Mirabilis expansa. Planta, 217, 498–506.

    Article  CAS  PubMed  Google Scholar 

  • Verma, H. N., Chowdhury, B., & Rastogi, P. (1984). Antiviral activity in leaf extracts of different Clerodendrum species. Journal of Plant Diseases and Protection, 91, 34–41.

    Google Scholar 

  • Verma, H. N., Srivastava, S., & Varsha, & Kumar, D. (1996). Induction of systemic resistance in plants against viruses by a basic protein from Clerodendrum aculeatum leaves. Phytopathology, 86, 485–492.

    Article  CAS  Google Scholar 

  • Vivanco, J. M., & Tumer, N. E. (2003). Translation inhibition of capped and uncapped viral RNAs mediated by ribosome-inactivating proteins. Phytopathology, 93, 588–595.

    Article  CAS  PubMed  Google Scholar 

  • Vivanco, J. M., Querci, M., & Salazar, L. F. (1999a). Antiviral and antiviroid activity of MAP containing extracts from Mirabilis jalapa roots. Plant Disease, 83, 1116–1121.

    Article  CAS  PubMed  Google Scholar 

  • Vivanco, J. M., Savary, B. J., & Flores, H. E. (1999b). Characterization of two novel type I ribosome-inactivating proteins from the storage roots of the Andean crop Mirabilis expansa. Plant Physiology, 119, 1447–1456.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walsh, M. J., Dodd, J. E., & Hautbergue, G. M. (2013). Ribosome-inactivating proteins: Potent poisons and molecular tools. Virulence, 4, 774–784.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, P., Zoubenko, O., & Tumer, N. E. (1998). Reduced toxicity and broad spectrum resistance to viral and fungal infection in transgenic plants expressing pokeweed antiviral protein II. Plant Molecular Biology, 38, 957–964.

    Article  CAS  PubMed  Google Scholar 

  • Wang, S., Li, Z., Li, S., Di, R., Ho, C. T., & Yang, G. (2016). Ribosome-inactivating proteins (RIPs) and their important health promoting property. RSC Advances, 6, 46794–46805.

    Article  CAS  Google Scholar 

  • Wong, J. H., Bao, H., Ng, T. B., Chan, H., Ng, C., Man, G., Wang, H., Guan, S., Zhao, S., Fang, E. F., Rolka, K., Liu, Q., Li, C., Sha, O., & Xia, L. (2020). New ribosome-inactivating proteins and other proteins with protein synthesis-inhibiting activities. Applied Microbiology and Biotechnology, 104, 4211–4226.

    Article  CAS  PubMed  Google Scholar 

  • Wu, X., Valli, A., García, J. A., Zhou, X., & Cheng, X. (2019). The tug-of-war between plants and viruses: Great progress and many remaining questions. Viruses, 11, 203.

    Article  CAS  PubMed Central  Google Scholar 

  • Yang, T., Meng, Y., Chen, L. J., Lin, H. H., & Xi, D. H. (2016). The roles of alpha-momorcharin and jasmonic acid in modulating the response of Momordica charantia to cucumber mosaic virus. Frontiers in Microbiology, 7, 1796.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang, T., Zhu, L. S., Meng, Y., Lv, R., Zhou, Z., Zhu, L., Lin, H. H., & Xi, D. H. (2018). Alpha-momorcharin enhances tobacco mosaic virus resistance in tobaccoNN by manipulating jasmonic acid-salicylic acid crosstalk. Journal of Plant Physiology, 223, 116–126.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, H., Tian, Y., Zhou, Y., Dang, B., Lan, H., Song, G., Wang, L., Liu, G., Zhang, L., & Chen, Z. (1999). Introduction of pokeweed antiviral protein cDNA into Brassica napus and acquisition of transgenic plants resistant to viruses. Chinese Science Bulletin, 44, 701–704.

    Article  CAS  Google Scholar 

  • Zhao, S., Lei, J. J., Chen, G. J., & Cao, B. H. (2008). Obtainment of transgenic mustard (Brassica juncea Coss.) with pokeweed antiviral protein gene and its resistance to TuMV. Journal of Agriculture Biotechnology, 16, 971–976.

    CAS  Google Scholar 

  • Zhu, F., Zhang, P., Meng, Y. F., Xu, F., Zhang, D. W., Cheng, J., Lin, H. H., & Xi, D. H. (2013). Alpha-momorcharin, a RIP produced by bitter melon, enhances defense response in tobacco plants against diverse plant viruses and shows antifungal activity in vitro. Planta, 237, 77–88.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, F., Yuan, S., Zhang, Z. W., Qian, K., Feng, J. G., & Yang, Y. Z. (2016). Pokeweed antiviral protein (PAP) increases plant systemic resistance to tobacco mosaic virus infection in Nicotiana benthamiana. European Journal of Plant Pathology, 146, 541–549.

    Article  CAS  Google Scholar 

  • Zhu, F., Zhou, Y. K., Ji, Z. L., & Chen, X. R. (2018). The plant ribosome-inactivating proteins play important roles in defense against pathogens and insect pest attacks. Frontiers in Plant Science, 9, 146.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu, F., Zhu, P., Xu, F., Che, Y., Ma, Y., & Ji, Z. L. (2020). Alpha-momorcharin enhances Nicotiana benthamiana resistance to tobacco mosaic virus infection through modulation of reactive oxygen species. Molecular Plant Pathology, 21, 1212–1226.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zoubenko, O., Hudak, K., & Tumer, N. E. (2000). A non-toxic pokeweed antiviral protein mutant inhibits pathogen infection via a novel salicylic acid-independent pathway. Plant Molecular Biology, 44, 219–229.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rajesh Kumar.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

This work does not contain any studies with human participants or animals performed by any of the authors.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 19 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, R., Bhattacharjee, A. & Tiwari, S. Plant-derived ribosome-inactivating proteins involved in defense against plant viruses. Eur J Plant Pathol 162, 515–537 (2022). https://doi.org/10.1007/s10658-021-02426-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-021-02426-1

Keywords

Navigation