Skip to main content

Advertisement

Log in

Genetic modification of crop plants with ribosome-inactivating protein genes for enhanced resistance to pathogens and pests

  • Review
  • Published:
Journal of Plant Diseases and Protection Aims and scope Submit manuscript

Abstract

Genetic engineering has emerged as an attractive strategy for incorporating resistance in plants against diverse pathogens and has been largely achieved through transgenic expression of ribosome-inactivating proteins (RIPs), pathogenesis-related (PR) proteins, pathogen-derived genes, or strategies involving RNA interference and clustered regularly interspaced short palindromic repeats/CRISPR-associated protein 9 (CRISPR/Cas9) gene editing tool. RIPs are rRNA N-glycosylases that commonly exert their protective effects through suppression of translation by enzymatically inactivating ribosomes, thereby arresting protein synthesis. Additionally, a few RIPs may possess other enzymatic activities viz. superoxide dismutase, chitinase, DNase and phosphatase, contributing towards pathogen resistance in plants. RIPs are mostly produced by plants and conventionally classified into three types. Type I RIPs are monomeric, with catalytic A chains, exhibiting rRNA N-glycosylase activity. Type II RIPs are dimeric, comprising the enzymatically active A chain associated with the lectin B chain enabling an access inside the cells, hence these are often highly toxic. Less common Type III RIPs include the jasmonic acid inducible protein such as JIP-60, with the catalytic domain becoming functional upon removal of an internal peptide segment and following cleavage of a C-terminal domain which resembles the eukaryotic initiation factor 4e. Unusual RIPs and RIP-related proteins, that cannot be grouped into the classical three types of RIPs, because of their difference in size, structure, or function, also exist. Several RIPs have been recombinantly expressed and demonstrated to possess catalytic activity. Plants carrying RIP transgenes exhibit resistance against viruses, fungi and insects. More often, such studies have been carried out using model systems comprising tobacco, potato or tomato, transformed via Agrobacterium tumefaciens, and employing the most widely used promoter such as CaMV 35S, to enable a high-level expression of the RIP gene. This review focuses on the recent developments in the recombinant DNA approach for the modification of crops with RIP genes to reduce the impact of pathogens and pests.

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
Fig. 2

Similar content being viewed by others

References

  • Ajji PK, Walder K, Puri M (2016) Functional analysis of a type-I ribosome inactivating protein balsamin from Momordica balsamina with anti-microbial and DNase activity. Plant Foods Hum Nutr 71:265–271

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Balasubrahmanyam A, Baranwal VK, Lodha ML, Varma A, Kapoor HC (2000) Purification and properties of growth stage-dependent antiviral proteins from the leaves of Celosia cristata. Plant Sci 154:13–21

    Article  CAS  PubMed  Google Scholar 

  • Balconi C, Lanzanova C, Conti E, Triulzi T, Forlani F, Cattaneo M, Lupotto E (2007) Fusarium head blight evaluation in wheat transgenic plants expressing the maize b-32 antifungal gene. Eur J Plant Pathol 117:129–140

    Article  CAS  Google Scholar 

  • Baranwal VK, Tumer NE, Kapoor HC (2002) Depurination of ribosomal RNA and inhibition of viral RNA translation by an antiviral protein of Celosia cristata. Indian J Exp Biol 40:1195–1197

    CAS  PubMed  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 Res 25:518–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbieri L, Polito L, Bolognesi A, Ciani M, Pelosi E, Farini V, Jha AK, Sharma N, Vivanco JM, Chambery A, Parente A, Stirpe F (2006) Ribosome-inactivating proteins in edible plants and purification and characterization of a new ribosome-inactivating protein from Cucurbita moschata. Biochim Biophys Acta 1760:783–792

    Article  CAS  PubMed  Google Scholar 

  • Begam M, Narwal S, Roy S, Kumar S, Lodha ML, Kapoor HC (2006) An antiviral protein having deoxyribonuclease and ribonuclease activity from leaves of the post-flowering stage of Celosia cristata. Biochem (Moscow) 71:S44–S48

    Article  CAS  Google Scholar 

  • Bertholdo-Vargas LR, Martins JN, Bordin D, Salvador M, Schafer AE, Barros NM, Barbieri L, Stirpe F, Carlini CR (2009) Type 1 ribosome-inactivating proteins - entomotoxic, oxidative and genotoxic action on Anticarsia gemmatalis (Hübner) and Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae). J Insect Physiol 55:51–58

    Article  CAS  PubMed  Google Scholar 

  • Bhatia S, Lodha ML (2005) RNase and DNase activities of antiviral proteins from leaves of Bougainvillea xbuttiana. Ind J Biochem Biophys 42:152–155

    CAS  Google Scholar 

  • Bhatia S, Kapoor HC, Lodha ML (2004) Modification of antioxidant status of host cell in response to Bougainvillea antiviral proteins. J Plant Biochem Biotechnol 18:113–119

    Article  Google Scholar 

  • Bieri S, Potrykus I, Fütterer J (2000) Expression of active barley seed ribosome-inactivating protein in transgenic wheat. Theor Appl Genet 100:755–763

    Article  CAS  Google Scholar 

  • Bolognesi A, Polito L, Olivieri F, Valbonesi P, Barbieri L, Battelli MG, Carusi MV, Benvenuto E, Del Vecchio BF, 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, Polito L, Lubelli C, Barbieri L, Parente A, Stirpe F (2002) Ribosome-inactivating and adenine polynucleotide glycosylase activities in Mirabilis jalapa L. tissues. J Biol Chem 277:13709–13716

    Article  CAS  PubMed  Google Scholar 

  • Broekaert WF, Nsimba-Lubaki M, Peeters B, Peumans WJ (1984) A lectin from elder (Sambucus nigra L.) bark. Biochem J 221:163–169

    Article  CAS  PubMed  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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). Afr J Biotechnol 10:6883–6890

    CAS  Google Scholar 

  • Carzaniga R, Sinclair L, Fordham-Skelton AP, Harris N, Croy RRD (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 

  • Cavalieri A, Czapla T, Howard J, Rao G (1995) Larvicidal lectins and plant insect resistance based thereon. U.S. Patent 5407454

  • Chaudhry B, Müller-Uri F, Cameron-Mills V, Gough S, Simpson D, Skriver K, Mundy J (1994) The barley 60 kDa jasmonate-induced protein (JIP60) is a novel ribosome-inactivating protein. Plant J 6:815–824

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, White RF, Antoniw JF, Lin Q (1991) Effect of pokeweed antiviral protein (PAP) on the infection of plant viruses. Plant Pathol 40:612–620

    Article  Google Scholar 

  • Chen Z, Antoniw JF, White RF (1993) A possible mechanism for the antiviral activity of pokeweed antiviral protein. Physiol Mol Plant Pathol 42:249–258

    Article  CAS  Google Scholar 

  • Chen H, Wang Y, Yan M, Yu M, Yao Q (1996) 5’-AMP phosphatase activity on trichosanthin and other single chain ribosome inactivating proteins. Chin Biochem J 12:125–130

    CAS  Google Scholar 

  • Chen Y, Peumans WJ, Van Damme EJM (2002) The Sambucus nigra type-2 ribosome-inactivating protein SNA-I’ exhibits in planta antiviral activity in transgenic tobacco. FEBS Lett 516:27–30

    Article  CAS  PubMed  Google Scholar 

  • Chen GJ, Shi L, Lei JJ, Cao BH, Zeng GP (2008) Cloning of pokeweed antiviral protein gene from Phytolacca acinosa and its transfer to pepper (Capsicum annuum L.). Acta Hortic Sin 35:847–852

    CAS  Google Scholar 

  • Chhikara S, Chaudhury D, Dhankher OP, Jaiwal PK (2012) Combined expression of a barley class II chitinase and type I ribosome inactivating protein in transgenic Brassica juncea provides protection against Alternaria brassicae. Plant Cell Tissue Organ Cult 108:83–89

    Article  CAS  Google Scholar 

  • Cho KJ, Lee SM, Kim YT, Hwang YS (2000) Purification and characterization of an antiviral ribosome-inactivating protein from Chenopodium album L. J Appl Biol Chem 43:125–130

    CAS  Google Scholar 

  • Chopra R, Saini R (2014) Transformation of blackgram (Vigna mungo (L.) Hepper) by barley chitinase and ribosome-inactivating protein genes towards improving resistance to Corynespora leaf spot fungal disease. Appl Biochem Biotechnol 174:2791–2800

    Article  CAS  PubMed  Google Scholar 

  • Choudhary N, Kapoor HC, Lodha ML (2008a) Cloning and expression of antiviral/ribosome-inactivating protein from Bougainvillea xbuttiana. J Biosci 33:91–101

    Article  CAS  PubMed  Google Scholar 

  • Choudhary N, Yadav OP, Lodha ML (2008b) Ribonuclease, deoxyribonuclease and antiviral activity of Escherichia coli-expressed Bougainvillea xbuttiana antiviral protein 1. Biochem Mosc 73:273–277

    Article  CAS  Google Scholar 

  • Choudhary N, Lodha ML, Baranwal VK (2020) The role of enzymatic activities of antiviral proteins from plants for action against plant pathogens. 3 Biotech 10:505

    Article  PubMed  PubMed Central  Google Scholar 

  • Citores L, Iglesias R, Gay C, Ferreras JM (2016) Antifungal activity of the ribosome-inactivating protein BE27 from sugar beet (Beta vulgaris L.) against the green mould Penicillium digitatum. Mol Plant Pathol 17:261–271

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corrado G, Bovi PD, Ciliento R, Gaudio L, Di Maro A, Aceto S, Lorito M, Rao R (2005) Inducible expression of a Phytolacca heterotepala ribosome-inactivating protein leads to enhanced resistance against major fungal pathogens in tobacco. Phytopathology 95:206–215

    Article  CAS  PubMed  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 Sci 174:467–474

    Article  CAS  Google Scholar 

  • Dai W, Bonos S, Guo Z, Meyer W, Day P, Belanger F (2003) Expression of pokeweed antiviral proteins in creeping bentgrass. Plant Cell Rep 21:497–502

    Article  CAS  PubMed  Google Scholar 

  • De Zaeytijd J, Rouge P, Smagghe G, Van Damme EJM (2019) Structure and activity of a cytosolic ribosome-inactivating protein from rice. Toxins 11:325

    Article  PubMed  PubMed Central  Google Scholar 

  • De Zaeytijd J, Chen P, Scheys F, Subramanyam K, Dubiel M, De Schutter K, Smagghe G, Van Damme EJM (2020) Involvement of OsRIP1, a ribosome-inactivating protein from rice, in plant defense against Nilaparvata lugens. Phytochemistry 170:112190

    Article  PubMed  Google Scholar 

  • Desmyter S, Vandenbussche F, Hao Q, Proost P, Peumans WJ, Van Damme EJM (2003) Type-1 ribosome-inactivating protein from iris bulbs: a useful agronomic tool to engineer virus resistance? Plant Mol Biol 51:567–576

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Di R, Tumer NE (2005) Expression of a truncated form of ribosomal protein L3 confers resistance to pokeweed antiviral protein and the Fusarium mycotoxin deoxynivalenol. Mol Plant Microbe Interact 18:762–770

    Article  CAS  PubMed  Google Scholar 

  • Domashevskiy AV, Cheng SY (2015) Thermodynamic analysis of binding and enzymatic properties of pokeweed antiviral protein (PAP) toward tobacco etch virus (TEV) RNA. J Nat Sci 1:e82

    Google Scholar 

  • Dong OX, Ronald PC (2019) Genetic engineering for disease resistance in plants: recent progress and future perspectives. Plant Physiol 180:26–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dowd PF, Zuo WN, Gillikin JW, Johnson ET, Boston RS (2003) Enhanced resistance to Helicoverpa zea in tobacco expressing an activated form of maize ribosome-inactivating protein. J Agric Food Chem 51:3568–3574

    Article  CAS  PubMed  Google Scholar 

  • Dowd PF, Holmes RA, Pinkerton TS, Johnson ET, Lagrimini LM, Boston RS (2006) Relative activity of a tobacco hybrid expressing high levels of a tobacco anionic peroxidase and maize ribosome-inactivating protein against Helicoverpa zea and Lasioderma serricorne. J Agric Food Chem 54:2629–2634

    Article  CAS  PubMed  Google Scholar 

  • Dowd PF, Johnson ET, Price NP (2012) Enhanced pest resistance of maize leaves expressing monocot crop plant-derived ribosome-inactivating protein and agglutinin. J Agric Food Chem 60:10768–10775

    Article  CAS  PubMed  Google Scholar 

  • Dutt S, BalasubrahmanyamLodha AM (2000) Purification and partial characterization of antiviral proteins from Chenopodium album L. leaves. J Plant Physiol 156:808–810

    Article  CAS  Google Scholar 

  • Dutt S, Narwal S, Kapoor HC, Lodha ML (2003) Isolation and characterization of two protein isoforms with antiviral activity from Chenopodium album L. leaves. J Plant Biochem Biotechnol 12:117–122

    Article  CAS  Google Scholar 

  • Dutt S, Yadav OP, Kapoor HC, Lodha ML (2004) Possible mechanism of action of antiviral proteins from the leaves of Chenopodium album L. Indian J Biochem Biophys 41:29–33

    CAS  PubMed  Google Scholar 

  • Endo Y, Tsurugi K (1987) RNA N-glycosidase activity of ricin A-chain. Mechanism of action of the toxic lectin ricin on eukaryotic ribosomes. J Biol Chem 262:8128–8130

    Article  CAS  PubMed  Google Scholar 

  • Fong WP, Mock WY, Ng TB (2000) Intrinsic ribonuclease activities in ribonuclease and ribosome-inactivating proteins from the seeds of bitter gourd. Int J Biochem Cell Biol 32:571–577

    Article  CAS  PubMed  Google Scholar 

  • Fu DL, Wang LL, Zhang HY, Chen ZH (2000) Introduction of PAP cDNA into potato by the laser microbeam puncture techniques. Acta Photonica Sin 29:970–974

    Google Scholar 

  • Gandhi R, Manzoor M, Hudak KA (2008) Depurination of brome mosaic virus RNA3 in vivo results in translation-dependent accelerated degradation of the viral RNA. J Biol Chem 283:32218–32228

    Article  CAS  PubMed  Google Scholar 

  • Gatehouse AMR, Barbieri L, Stirpe F, Croy RRD (1990) Effects of ribosome inactivating proteins on insect development differences between Lepidoptera and Coleoptera. Entomol Exp Appl 54:43–51

    Article  CAS  Google Scholar 

  • Gholizadeh A (2019) Purification of a ribosome-inactivating protein with antioxidation and root developer potencies from Celosia plumosa. Physiol Mol Biol Plants 25:243–251

    Article  CAS  PubMed  Google Scholar 

  • Gholizadeh A, Kumar M, Balasubrahmanyam A, Sharma S, Narwal S, Lodha ML, Kapoor HC (2004) Antioxidant activity of antiviral proteins from Celosia cristata. J Plant Biochem Biotechnol 13:13–18

    Article  CAS  Google Scholar 

  • Girbés T, Ferreras JM, Arias FJ, Stirpe F (2004) Description, distribution, activity and phylogenetic relationship of ribosome-inactivating proteins in plants, fungi and bacteria. Mini Rev Med Chem 4:461–476

    Article  CAS  PubMed  Google Scholar 

  • Gonzales-Salazar R, Cecere B, Ruocco M, Rao R, Corrado G (2017) A comparison between constitutive and inducible transgenic expression of the PhRIP I gene for broad-spectrum resistance against phytopathogens in potato. Biotechnol Lett 39:1049–1058

    Article  CAS  PubMed  Google Scholar 

  • Guller A, Sipahioğlu HM, Usta M, Durak ED (2018) Antiviral and antifungal activity of biologically active recombinant bouganin protein from Bougainvillea spectabilis willd. J Agric Sci 24:227–237

    Google Scholar 

  • Hamshou M, Shang C, Smagghe G, Van Damme EJM (2016) Ribosome-inactivating proteins from apple have strong aphicidal activity in artificial diet and in planta. Crop Prot 87:19–24

    Article  CAS  Google Scholar 

  • Hamshou M, Shang C, De Zaeytijd J, Van Damme EJ, Smagghe G (2017) Expression of ribosome-inactivating proteins from apple in tobacco plants results in enhanced resistance to Spodoptera exigua. J Asia-Pac Entomol 20:1–5

    Article  Google Scholar 

  • Hartley MR, Chaddock JA, Bonness MS (1996) The structure and function of ribosome inactivating proteins. Trends Plant Sci 1:254–260

    Article  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. Agric Biol Chem 51:897–904

    CAS  Google Scholar 

  • Hong Y, Saunders K, Hartley MR, 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 

  • Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT (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 Regul 54:115–123

    Article  CAS  Google Scholar 

  • Hudak KA, Wang P, Tumer NE (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 JM, Antolín P, Jiménez P, Rojo MA, Méndez E, Girbés T (2005) Molecular characterization and systemic induction of single-chain ribosome-inactivating proteins (RIPs) in sugar beet (Beta vulgaris) leaves. J Exp Bot 56:1675–1684

    Article  CAS  PubMed  Google Scholar 

  • Iglesias R, Citores L, Di Maro A, Ferreras JM (2015) Biological activities of the antiviral protein BE27 from sugar beet (Beta vulgaris L.). Planta 241:421–433

    Article  CAS  PubMed  Google Scholar 

  • Iglesias R, Citores L, Ragucci S, Russo R, Di Maro A, Ferreras JM (2016) Biological and antipathogenic activities of ribosome-inactivating proteins from Phytolacca dioica L. Biochim Biophys Acta 1860:1256–1264

    Article  CAS  PubMed  Google Scholar 

  • Irvin JD, Kelly T, Robertus JD (1980) Purification and properties of a second antiviral protein from Phytolacca americana which inactivates eukaryotic ribosomes. Arch Biochem Biophys 200:418–425

    Article  CAS  PubMed  Google Scholar 

  • ISAAA (2019) Global status of commercialized biotech/GM crops in 2019: biotech crops drive socio-economic development and sustainable environment in the new frontier. ISAAA Brief No. 55. ISAAA: Ithaca, NY

  • Jach G, Görnhardt B, Mundy J, Logemann J, Pinsdorf E, Leah R, Schell J, Maas C (1995) Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. Plant J 8:97–109

    Article  CAS  PubMed  Google Scholar 

  • Jiang GY, Weng ML, Jin DM, Wang B (1998) Characteristics of TCS transgenic tomato. Acta Hortic Sin 25:395–396

    Google Scholar 

  • Jiang GY, Jin DM, Weng ML, Guo BT, Wang B (1999) Transformation and expression of trichosanthin gene in tomato. Acta Bot Sin 41:334–336

    CAS  Google Scholar 

  • Karran RA, Hudak KA (2008) Depurination within the intergenic region of brome mosaic virus RNA3 inhibits viral replication in vitro and in vivo. Nucleic Acids Res 36:7230–7239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karran RA, Hudak KA (2011) Depurination of brome mosaic virus RNA3 inhibits its packaging into virus particles. Nucleic Acids Res 39:7209–7222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaur S, Samota MK, Choudhary M, Choudhary M, Pandey AK, Sharma A, Thakur J (2022) How do plants defend themselves against pathogens—Biochemical mechanisms and genetic interventions. Physiol Mol Biol Plants 28:485–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JK, Jang IC, Wu R, Zuo WN, Boston RS, Lee YH, Ahn IP, Nahm BH (2003) Co-expression of a modified maize ribosome-inactivating protein a rice basic chitinase gene in transgenic rice plants confers enhanced resistance to sheath blight. Transgenic Res 12:475–484

    Article  CAS  PubMed  Google Scholar 

  • Kim YS, Park SC, Oh SK, Lee H, Cho JW, Chung CH (1999a) Antiviral proteins, amarandin 1 and 2, from Amaranthus viridis, DNAs encoding therefrom. United States Patent No. 6001986-A

  • Kim YS, Park SC, Oh SK, Lee H, Cho JW, Chung CH (1999b) DNA encoding amarandin-S ribosome inactivating protein of Amaranthus viridis. United States Patent No. 5977335-A

  • Krishnan R, McDonald KA, Dandekar AM, Jackman AP, Falk B (2002) Expression of recombinant trichosanthin, a ribosome-inactivating protein, in transgenic tobacco. J Biotechnol 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. Ann Phytopath Soc Japan 56:481–487

    Article  Google Scholar 

  • Kumar MA, Timm DE, Neet KE, Owen WG, Peumans WJ, Rao AG (1993) Characterization of the lectin from the bulbs of Eranthis hyemalis (winter aconite) as an inhibitor of protein synthesis. J Biol Chem 268:25176–25183

    Article  CAS  PubMed  Google Scholar 

  • Kumar R, Bhattacharjee A, Tiwari S (2022) Plant-derived ribosome-inactivating proteins involved in defense against plant viruses. Eur J Plant Pathol 162:515–537

    Article  CAS  Google Scholar 

  • Kushwaha GS, Pandey N, Sinha M, Singh SB, Kaur P, Sharma S, Singh TP (2012) Crystal structures of a type-1 ribosome inactivating protein from Momordica balsamina in the bound and unbound states. Biochim Biophys Acta 1824:679–691

    Article  CAS  PubMed  Google Scholar 

  • Kwon SY, An CS, Liu JR, Paek KH (1997) A ribosome-inactivating protein from Amaranthus viridis. Biosci Biotechnol Biochem 61:1613–1614

    Article  CAS  PubMed  Google Scholar 

  • Kwon SY, An CS, Liu JR, Kwak SS, Lee HS, Kim JK, Paek KH (2000) Molecular cloning of a cDNA encoding ribosome inactivating protein from Amaranthus viridis and its expression in E. coli. Mol Cells 10:8–12

    Article  CAS  PubMed  Google Scholar 

  • Lam YH, Wong YS, Wang B, Wong RNS, Yeung HW, Shaw PC (1996) Use of trichosanthin to reduce infection by turnip mosaic virus. Plant Sci 114:111–117

    Article  CAS  Google Scholar 

  • Landi N, Ragucci S, Citores L, Clemente A, Hussain HZF, Iglesias R, Ferreras JM, Di Maro A (2022) Isolation, characterization and biological action of type-1 ribosome-inactivating proteins from tissues of Salsola soda L. Toxins (basel) 14:566

    Article  CAS  PubMed  Google Scholar 

  • Lanzanova C, Giuffrida MG, Motto M, Baro C, Donn G, Hartings H, Lupotto E, Careri M, Elviri L, Balconi C (2009) The Zea mays b-32 ribosome-inactivating protein efficiently inhibits growth of Fusarium verticillioides on leaf pieces in vitro. Eur J Plant Pathol 124:471–482

    Article  CAS  Google Scholar 

  • Leah R, Tommerup H, Svendsen I, Mundy J (1991) Biochemical and molecular characterization of three barley seed proteins with antifungal properties. J Biol Chem 266:1564–1573

    Article  CAS  PubMed  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. J Appl Biol Chem 42:161–165

    CAS  Google Scholar 

  • Li XD, Chen WF, Liu WY, Wang GH (1997) Large-scale preparation of two new ribosome-inactivating proteins–cinnamomin and camphorin from the seeds of Cinnamomum camphora. Protein Expr Purif 10:27–31

    Article  CAS  PubMed  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. J Integr Plant Biol 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. J Phytopathol 161:239–245

    Article  CAS  Google Scholar 

  • Lin JY, Kao WY, Tserng KY, Chen CC, Tung TC (1970) Effect of crystalline abrin on the biosynthesis of protein, RNA, and DNA in experimental tumors. Cancer Res 30:2431–2433

    CAS  PubMed  Google Scholar 

  • Lodge JK, Kaniewski WK, Tumer NE (1993) Broad-spectrum virus resistance in transgenic plants expressing pokeweed antiviral protein. Proc Natl Acad Sci USA 90:7089–7093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lodha ML, Agarwal S, Biswas K, Vasudev S, Dubey SC (2010) Antimicrobial activity of native and recombinant antiviral proteins from Bougainvillea xbuttiana leaves against plant pathogenic fungi and viruses. Indian J Agric Biochem 23:83–90

    CAS  Google Scholar 

  • Logemann J, Jach G, Tommerup H, Mundy J, Schell J (1992) Expression of a barley ribosome-inactivating protein leads to increased fungal protection in transgenic tobacco plants. Nat Biotechnol 10:305–308

    Article  CAS  Google Scholar 

  • Lombard S, Helmy ME, Piéroni G (2001) Lipolytic activity of ricin from Ricinus sanguineus and Ricinus communis on neutral lipids. Biochem J 358:773–781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maddaloni M, Forlani F, Balmas V, Donini G, Stasse L, Corazza L, Motto M (1997) Tolerance to the fungal pathogen Rhizoctonia solani AG4 of transgenic tobacco expressing the maize ribosome-inactivating protein b-32. Transgenic Res 6:393–402

    Article  CAS  Google Scholar 

  • M’hamdi M, Rouhou HC, Boughalleb N, deGalarretaGómez JIR (2012) Enhanced resistance to Rhizoctonia solani by combined expression of chitinase and ribosome inactivating protein in transgenic potatoes (Solanum tuberosum L.). Span J Agric Res 10:778–785

    Article  Google Scholar 

  • Moon YH, Jeon HS, Choi KW, Lee JS (1994) Development of virus-resistant potato by expression of Phytolacca antiviral protein. Mol Cells 4:183–188

    CAS  Google Scholar 

  • Moon YH, Song SK, Choi KW, Lee JS (1997) Expression of a cDNA encoding Phytolacca insularis antiviral protein confers virus resistance on transgenic potato plants. Mol Cells 7:807–815

    CAS  PubMed  Google Scholar 

  • Narwal S, Balasubrahmanyam A, Lodha ML, Kapoor HC (2001a) Purification and properties of antiviral proteins from the leaves of Bougainvillea xbuttiana. Indian J Biochem Biophys 38:342–347

    CAS  PubMed  Google Scholar 

  • Narwal S, Balasubrahmanyam A, Sadhna P, Kapoor HC, Lodha ML (2001b) A systemic resistance inducing antiviral protein with N-glycosidase activity from Bougainvillea xbuttiana leaves. Indian J Exp Biol 39:600–603

    CAS  PubMed  Google Scholar 

  • Ng TB, Parkash A (2002) Hispin, a novel ribosome inactivating protein with antifungal activity from hairy melon seeds. Protein Expr Purif 26:211–217

    Article  CAS  PubMed  Google Scholar 

  • Ng TB, Parkash A, Tso WW (2003) Purification and characterization of alpha- and beta-benincasins, arginine/glutamate-rich peptides with translation-inhibiting activity from wax gourd seeds. Peptides 24:11–16

    Article  CAS  PubMed  Google Scholar 

  • Noman A, Aqeel M, Islam W, Khalid N, Akhtar N, Qasim M, Yasin G et al (2021) Insects–plants-pathogens: toxicity, dependence and defense dynamics. Toxicon 197:87–98

    Article  CAS  PubMed  Google Scholar 

  • Oerke EC (2006) Crop losses to pests. J Agric Sci 144:31–43

    Article  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 Lett 396:132–134

    Article  CAS  PubMed  Google Scholar 

  • Olsnes S, Pihl A (1972) Ricin—a potent inhibitor of protein synthesis. FEBS Lett 20:327–329

    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. Agric Biol Chem 51:891–896

    CAS  Google Scholar 

  • Parkash A, Ng TB, Tso WW (2002) Isolation and characterization of luffacylin, a ribosome inactivating peptide with anti-fungal activity from sponge gourd (Luffa cylindrica) seeds. Peptides 23:1019–1024

    Article  CAS  PubMed  Google Scholar 

  • Picard D, Kao CC, Hudak KA (2005) Pokeweed antiviral protein inhibits brome mosaic virus replication in plant cells. J Biol Chem 280:20069–20075

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Prasad V, Mishra SK, 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 Rep 33:1467–1478

    Article  CAS  PubMed  Google Scholar 

  • Qian Q, Huang L, Yi R, Wang S, Ding Y (2014) Enhanced resistance to blast fungus in rice (Oryza sativa L.) by expressing the ribosome-inactivating protein alpha-momorcharin. Plant Sci 217:1–7

    Article  PubMed  Google Scholar 

  • Ragucci S, Bulgari D, Landi N, Russo R, Clemente A, Valletta M, Chambery A, Gobbi E, Faoro F, Di Maro A (2021) The structural characterization and antipathogenic activities of quinoin, a type 1 ribosome-inactivating protein from quinoa seeds. Int J Mol Sci 22:8964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ready MP, Brown DT, Robertus JD (1986) Extracellular localization of pokeweed antiviral protein. Proc Natl Acad Sci U S A 83:5053–5056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rezaei-Moshaei M, Dehestani A, Bandehagh A, Pakdin-Parizi A, Golkar M, Heidari-Japelaghi R (2021) Recombinant pebulin protein, a type 2 ribosome-inactivating protein isolated from dwarf elder (Sambucus ebulus L.) shows anticancer and antifungal activities in vitro. Int J Biol Macromol 174:352–361

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ruan XL, Liu LF, Li H (2007) Transgenic tobacco plants with ribosome inactivating protein gene cassin from Cassia occidentalis and their resistance to tobacco mosaic virus. Zhi Wu Sheng Li Yu Fen Zi Sheng Wu XueXue Bao J Plant Physiol Molecul Biol 33:517–523

    CAS  Google Scholar 

  • Ruggiero A, Chambery A, Di Maro A, Mastroianni A, Parente A, Berisio R (2007) Crystallization and preliminary X-ray diffraction analysis of PD-L1, a highly glycosylated ribosome inactivating protein with DNase activity. Protein Pept Lett 14:407–409

    Article  CAS  PubMed  Google Scholar 

  • Sargolzaei M, Ho CL, Wong MY (2016) Characterization of novel type I ribosome-inactivating proteins isolated from oil palm (Elaeis guineensis) inoculated with Ganoderma boninense the causal agent of basal stem rot. Physiol Mol Plant Pathol 94:53–61

    Article  CAS  Google Scholar 

  • Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A (2019) The global burden of pathogens and pests on major food crops. Nat Ecol Evol 3:430–439

    Article  PubMed  Google Scholar 

  • Schrot J, Weng A, Melzig MF (2015) Ribosome-Inactivating and Related Proteins. Toxins 7:1556–1615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shahidi-Noghabi S, Van Damme EJM, Smagghe G (2008) Carbohydrate-binding activity of the type-2 ribosomes-inactivating protein SNA-I from elderberry (Sambucus nigra) is a determining factor for its insecticidal activity. Phytochemistry 69:2972–2978

    Article  CAS  PubMed  Google Scholar 

  • Shahidi-Noghabi S, Van Damme EJM, Smagghe G (2009) Expression of Sambucus nigra agglutinin (SNA-I′) from elderberry bark in transgenic tobacco plants results in enhanced resistance to different insect species. Transgenic Res 18:249–259

    Article  CAS  PubMed  Google Scholar 

  • Shahidi-Noghabi S, van Damme EJM, Iga M, Smagghe G (2010) Exposure of insect midgut cells to Sambucus nigra L. agglutinins I and II causes cell death via caspase-dependent apoptosis. J Insect Physiol 56:1101–1107

    Article  CAS  PubMed  Google Scholar 

  • Sharma N, Park SW, Vepachedu R, Barbieri L, Ciani M, Stirpe F, Savary BJ, Vivanco JM (2004) Isolation and characterization of an rip (ribosome-inactivating protein)-like protein from tobacco with dual enzymatic activity. Plant Physiol 134:171–181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shih NR, McDonald KA, Jackman AP, Girbés T, Iglesias R (1997) Bifunctional plant defence enzymes with chitinase and ribosome inactivating activities from Trichosanthes kirilowii cell cultures. Plant Sci 130:145–150

    Article  CAS  Google Scholar 

  • Sipahioglu HM, 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. Turk J Agric for 41:256–262

    Article  CAS  Google Scholar 

  • Smirnov S, Shulaev V, Tumer NE (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 Physiol 114:1113–1121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song SK, Choi Y, Moon YH, Kim SG, Choi YD, Lee JS (2000) Systemic induction of a Phytolacca insularis antiviral protein gene by mechanical wounding, jasmonic acid, and abscisic acid. Plant Mol Biol 43:439–450

    Article  CAS  PubMed  Google Scholar 

  • Srivastava A, Trivedi S, Krishna SK, Verma HN, Prasad V (2009) Suppression of papaya ringspot virus infection in Carica papaya with CAP-34, a systemic antiviral resistance inducing protein from Clerodendrum aculeatum. Eur J Plant Pathol 123:241–246

    Article  CAS  Google Scholar 

  • Srivastava S, Verma HN, Srivastava A, Prasad V (2015) BDP-30, a systemic resistance inducer from Boerhaavia diffusa L., suppresses TMV infection, and displays homology with ribosome-inactivating proteins. J Biosci 40:125–135

    Article  CAS  PubMed  Google Scholar 

  • Stirpe F, Battelli MG (2006) Ribosome-inactivating proteins: progress and problems. Cell Mol Life Sci 63:1850–1866

    Article  CAS  PubMed  Google Scholar 

  • Stirpe F, Williams DG, Onyon LJ, Legg RF, Stevens WA (1981) Dianthins, ribosome-damaging proteins with anti-viral properties from Dianthus caryophyllus L. (carnation). Biochem J 195:399–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Straub P, Adam G, Mundry KW (1986) Isolation and characterization of a virus inhibitor from spinach (Spinacia oleracea L.). J Phytopathol 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. Ann Phytopathol Soc Japan 56:488–494

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Torky ZA (2012) Isolation and characterization of antiviral protein from Salsola longifolia leaves expressing polynucleotide adenosine glycoside activity. Online J Sci Technol 2:52–58

    Google Scholar 

  • Tumer NE, Hwang DJ, Bonness M (1997) C-terminal deletion mutant of pokeweed antiviral protein inhibits viral infection but does not depurinate host ribosomes. Proc Natl Acad Sci USA 94:3866–3871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Damme EJ, Barre A, Rougé P, Van Leuven F, Peumans WJ (1996) The NeuAc(alpha-2,6)-Gal/GalNAc-binding lectin from elderberry (Sambucus nigra) bark, a type-2 ribosome-inactivating protein with an unusual specificity and structure. Eur J Biochem 235:128–137

    Article  PubMed  Google Scholar 

  • Van Damme EJ, Roy S, Barre A, Citores L, Mostafapous K, Rougé P, Van Leuven F, Girbés T, Goldstein IJ, Peumans WJ (1997) Elderberry (Sambucus nigra) bark contains two structurally different Neu5Ac(alpha2,6)Gal/GalNAc-binding type 2 ribosome-inactivating proteins. Eur J Biochem 245:648–655

    Article  PubMed  Google Scholar 

  • Vandenbussche F, Desmyter S, Ciani M, Proost P, Peumans WJ, Van Damme EJ (2004a) Analysis of the in planta antiviral activity of elderberry ribosome-inactivating proteins. Eur J Biochem 271:1508–1515

    Article  CAS  PubMed  Google Scholar 

  • Vandenbussche F, Peumans WJ, Desmyter S, Proost P, Ciani M, Van Damme EJM (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 

  • Vargas LRB, Carlini CR (2014) Insecticidal and antifungal activities of ribosome-inactivating proteins. In: Stirpe F, Lappi DA (eds) Ribosome-inactivating proteins: Ricin and related proteins. Wiley Blackwell Press, NJ, USA, pp 212–222

    Chapter  Google Scholar 

  • Vepachedu R, Bais HP, Vivanco JM (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 HN, 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 JM, Tumer NE (2003) Translation inhibition of capped and uncapped viral RNAs mediated by ribosome-inactivating proteins. Phytopathology 93:588–595

    Article  CAS  PubMed  Google Scholar 

  • Vivanco JM, Querci M, Salazar LF (1999a) Antiviral and antiviroid activity of MAP-containing extracts from Mirabilis jalapa roots. Plant Dis 83:1116–1121

    Article  CAS  PubMed  Google Scholar 

  • Vivanco JM, Savary BJ, Flores HE (1999b) Characterization of two novel type I ribosome-inactivating proteins from the storage roots of the andean crop Mirabilis expansa. Plant Physiol 119:1447–1456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walsh TA, Morgan AE, Hey TD (1991) Characterization and molecular cloning of a proenzyme form of a ribosome-inactivating protein from maize. Novel mechanism of proenzyme activation by proteolytic removal of a 2.8-kilodalton internal peptide segment. J Biol Chem 266:23422–23427

    Article  CAS  PubMed  Google Scholar 

  • Wang HX, Ng TB (2000) Lagenin, a novel ribosome-inactivating protein with ribonucleolytic activity from bottle gourd (Lagenaria siceraria) seeds. Life Sci 67:2631–2638

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Zoubenko O, Tumer NE (1998) Reduced toxicity and broad spectrum resistance to viral and fungal infection in transgenic plants expressing pokeweed antiviral protein II. Plant Mol Biol 38:957–964

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Zhang Y, Liu H, He Y, Yan J, Wu Z, Ding Y (2012) Molecular cloning and functional analysis of a recombinant ribosome-inactivating protein (alpha-momorcharin) from Momordica charantia. Appl Microbiol Biotechnol 96:939–950

    Article  PubMed  Google Scholar 

  • Wang S, Zheng Y, Yan J, Zhu Z, Wu Z, Ding Y (2013) Alpha-momorcharin: a ribosome-inactivating protein from Momordica charantia, possessing DNA cleavage properties. Protein Pept Lett 20:1257–1263

    Article  CAS  PubMed  Google Scholar 

  • Wei GQ, Liu RS, Wang Q, Liu WY (2004) Toxicity of two type II ribosome-inactivating proteins (cinnamomin and ricin) to domestic silkworm larvae. Arch Insect Biochem Physiol 57:160–165

    Article  CAS  PubMed  Google Scholar 

  • Wong JH, Bao H, Ng TB, Chan HHL, Ng CCW, Man GCW, Wang H, Guan S, Zhao S, Fang EF, Rolka K, Liu Q, Li C, Sha O, Xia L (2020) New ribosome-inactivating proteins and other proteins with protein synthesis-inhibiting activities. Appl Microbiol Biotechnol 104:4211–4226

    Article  CAS  PubMed  Google Scholar 

  • Wytynck P, Lambin J, Chen S, Demirel Asci S, Verbeke I, De Zaeytijd J, Subramanyam K, Van Damme EJM (2021) Effect of RIP overexpression on abiotic stress tolerance and development of rice. Int J Mol Sci 22:1434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang T, Meng Y, Chen LJ, Lin HH, Xi DH (2016) The roles of alpha-momorcharin and jasmonic acid in modulating the response of Momordica charantia to cucumber mosaic virus. Front Microbiol 7:1796

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang T, Zhu LS, Meng Y, Lv R, Zhou Z, Zhu L, Lin HH, Xi DH (2018) Alpha-momorcharin enhances tobacco mosaic virus resistance in tobaccoNN by manipulating jasmonic acid-salicylic acid crosstalk. J Plant Physiol 223:116–126

    Article  CAS  PubMed  Google Scholar 

  • Yuan H, Ming X, Wang L, Hu P, An C, Chen Z (2002) Expression of a gene encoding trichosanthin in transgenic rice plants enhances resistance to fungus blast disease. Plant Cell Rep 20:992–998

    Article  CAS  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. Chin Sci Bull 44:701–704

    Article  CAS  Google Scholar 

  • Zhao S, Lei JJ, Chen GJ, Cao BH (2008) Obtainment of transgenic mustard (Brassica juncea Coss.) with pokeweed antiviral protein gene and its resistance to TuMV. J Agric Biotechnol 16:971–976

    CAS  Google Scholar 

  • Zhou X, Li XD, Yuan JZ, Tang ZH, Liu WY (2000) Toxicity of cinnamomin–a new type II ribosome-inactivating protein to bollworm and mosquito. Insect Biochem Mol Biol 30:259–264

    Article  CAS  PubMed  Google Scholar 

  • Zhu F, Zhang P, Meng YF, Xu F, Zhang DW, Cheng J, Lin HH, Xi DH (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 ZW, Qian K, Feng JG, Yang YZ (2016) Pokeweed antiviral protein (PAP) increases plant systemic resistance to tobacco mosaic virus infection in Nicotiana benthamiana. Eur J Plant Pathol 146:541–549

    Article  CAS  Google Scholar 

  • Zhu F, Zhou YK, Ji ZL, Chen XR (2018) The plant ribosome-inactivating proteins play important roles in defense against pathogens and insect pest attacks. Front Plant Sci 9:146

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu F, Zhu PX, Xu F, Che YP, Ma YM, Ji ZL (2020) Alpha-momorcharin enhances Nicotiana benthamiana resistance to tobacco mosaic virus infection through modulation of reactive oxygen species. Mol Plant Pathol 21:1212–1226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zoubenko O, Uckun F, Hur Y, Chet I, Tumer N (1997) Plant resistance to fungal infection induced by nontoxic pokeweed antiviral protein mutants. Nat Biotechnol 15:992–996

    Article  CAS  PubMed  Google Scholar 

  • Zoubenko O, Hudak K, Tumer NE (2000) A non-toxic pokeweed antiviral protein mutant inhibits pathogen infection via a novel salicylic acid-independent pathway. Plant Mol Biol 44:219–229

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vivek Prasad.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, R., Srivastava, S. & Prasad, V. Genetic modification of crop plants with ribosome-inactivating protein genes for enhanced resistance to pathogens and pests. J Plant Dis Prot 130, 669–687 (2023). https://doi.org/10.1007/s41348-023-00713-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s41348-023-00713-z

Keywords

Navigation