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The role of enzymatic activities of antiviral proteins from plants for action against plant pathogens

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Abstract

Antiviral proteins (AVPs) from plants possess multiple activities, such as N-glycosidase, RNase, DNase enzymatic activity, and induce pathogenesis-related proteins, salicylic acid, superoxide dismutase, peroxidase, and catalase. The N-glycosidase activity releases the adenine residues from sarcin/ricin (S/R) loop of large subunit of ribosomes and interfere the host protein synthesis process and this activity has been attributed for antiviral activity in plant. It has been shown that AVP binds directly to viral genome-linked protein of plant viruses and interfere with protein synthesis of virus. AVPs also possess the RNase and DNase like activity and may be targeting nucleic acid of viruses directly. Recently, the antifungal, antibacterial, and antiinsect properties of AVPs have also been demonstrated. Gene encoding for AVPs has been used for the development of transgenic resistant crops to a broad range of plant pathogens and insect pests. However, the cytotoxicity has been observed in transgenic crops using AVP gene in some cases which can be a limiting factor for its application in agriculture. In this review, we have reviewed various aspects of AVPs particularly their characteristics, possible mode of action and application.

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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

    CAS  PubMed  Google Scholar 

  • Akkouh O, Ng TB, Cheung RC, Wong JH, Pan W, Ng CC, Sha O, Shaw PC, Chan WY (2015) Biological activities of ribosome-inactivating proteins and their possible applications as antimicrobial, anticancer, and anti-pest agents and in neuroscience research. Appl Microbiol Biotechnol 99:9847–9863

    CAS  PubMed  Google Scholar 

  • Balasaraswathi R, Sadasivam S, Chita HE, Raja JA (2001) Inhibition of in vitro translation and cleavage of rRNA by Bougainvillea antiviral protein. Indian J Agric Biochem 14:67–68

    CAS  Google Scholar 

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

    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 Celeosia cristata. Plant Sci 154:13–21

    CAS  PubMed  Google Scholar 

  • Baranwal VK, Verma HN (1992) Localized resistance against virus infection by leaf extract of Celosia cristata. Plant Pathol 41:633–638

    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, Aron GM, Irvin JD, Stirpe F (1982) Purification and partial characterization of another form of the antiviral protein from the seeds of Phytolacca americana L. (pokeweed). Biochem J 203:55–59

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barbieri L, Battelli MG, Stripe F (1993) Ribosome-inactivating proteins from plants. Biochem Biophys Acta 1554:237–282

    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). Nucl Acids Res 25:518–522

    CAS  PubMed  Google Scholar 

  • Barbieri L, Valbonesi P, Gorini P, Pession A, Stripe F (1996) Polynucleotide: adenosine glycosidase activity of saporin L1: effect on DNA RNA Poly(A). Biochem J 319:507–513

    CAS  PubMed  PubMed Central  Google Scholar 

  • Begam M, Sharma SK, Roy S, Campanella JJ, Kapoor HC (2006) Molecular cloning and functional identification of an antiviral/ribosome-inactivating protein from leaves of post-flowering stage of Celosia cristata. Phytochemistry 67:2441–2449

    CAS  PubMed  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 (JE Smith) (Lepidoptera: Noctuidae). J Insect Physiol 55:51–58

    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

    Google Scholar 

  • Bolognesi A, Polito L, Lubelli C, Barbieri L, Parente A, Stirpe F (2002) Ribosome-inactivating adenine polynucleotide glycosylase activities in Mirabilis jalapa L. tissues. J Biol Chem 277:13709–13716

    CAS  PubMed  Google Scholar 

  • Bolognesi A, Bortolotti M, Maiello S, Battelli MG, Polito L (2016) Ribosome-inactivating proteins from plants: a historical overview. Molecules 21:1627–1647

    PubMed Central  Google Scholar 

  • Bolognesi A, Polioto L, Olivieri F, Valbonesi P, Barbieri L, Batteli MG, Carusi MV, Benvenuto E, Blanco FDV, Maro AD, Parente AL, 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

    CAS  PubMed  Google Scholar 

  • Bornhoff BA, Harst M, Zyprian E, Topfer R (2005) Transgenic plants of Vitis vinifera cv Seyval blanc. Plant Cell Rep 24:433–438

    CAS  PubMed  Google Scholar 

  • Briddon RW, Markham PJ (2000) Cotton leaf curl virus disease. Virus Res 71:151–159

    CAS  PubMed  Google Scholar 

  • Chambery A, Di Maro A, Monti MM, Stirpe F, Parente A (2004) Volkensin from Adenia volkensii Harms (kilyambiti plant) a type 2 ribosome-inactivating protein. Eur J Biochem 271:108–117

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Cho HJ, Lee SJ, Kim S, Kim BD (2000) Isolation characterization of cDNAs encoding ribosome inactivating protein from Dianthus sinensis L. Mol Cells 10(2):135–141

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Citores L, de Benito FM, Iglesias R, Ferreras JM, Argueso P, Jimenez P, Testera A, Camafeita E, Mendez E, Girbes T (1997) Characterization of a new non-toxic two-chain ribosome-inactivating protein a structurally-related lectin from rhizomes of dwarf elder (Sambucus ebulus L.). Cell Mol Biol 43:485–499

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Das MK, Sharma RS, Mishra V (2012) Induction of apoptosis by ribosome inactivating proteins Importance of N-glycosidase activity. Appl Biochem Biotechnol 166:1552–1561

    CAS  PubMed  Google Scholar 

  • Dasgupta I, Malathi VG, Mukherjee SK (2003) Genetic engineering for virus resistance. Curr Sci 84:341–354

    CAS  Google Scholar 

  • Day PJ, Lord JM, Roberts LM (1998) The deoxyribonuclease activity attributed to ribosome-inactivating proteins is due to contamination. Eur J Biochem 258:540–545

    CAS  PubMed  Google Scholar 

  • Di Maro A, Valbonesi P, Bolognesi A, Stirpe F, DeLuca P, Siniscalco GG, Gaudio L, Delli BP, Ferranti P, Malorni A, Parente A (1999) Isolation and characterization of four type-1 ribosome-inactivating proteins with polynucleotide:adenosine glycosidase activity from leaves of Phytolaccadioica L. Planta 208:125–131

    PubMed  Google Scholar 

  • Di R, Tumer NE (2015) Pokeweed antiviral protein: its cytotoxicity mechanisms and applications in plant disease resistance. Toxins 7:755–772

    CAS  PubMed  PubMed Central  Google Scholar 

  • Domashevskiy AV, Goss DJ (2015) Pokeweed antiviral protein, a ribosome inactivating protein: activity, inhibition and prospects. Toxins (Basel) 7:274–298

    CAS  Google Scholar 

  • Domashevskiy AV, Miyoshi H, Goss DJ (2012) Inhibition of pokeweed antiviral protein (PAP) by turnip mosaic virus genome-linked protein (VPg). J Biol Chem 287:29729–29738

    CAS  PubMed  PubMed Central  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

    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 agglutinin. J Agric Food Chem 60:10768–10775

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Duggar BM, Armstrong JK (1925) The effect of treating the virus of tobacco mosaic with the juices of various plants. Ann Mo Botl Gard 12:359–366

    Google Scholar 

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

    CAS  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

    CAS  PubMed  Google Scholar 

  • Endo Y, Mitsui K, Motizuki M, Tsurugi K (1987) The mechanism of action of ricin and related toxic lectins on eukaryotic ribosomes. The site and the characteristics of the modification in 28S ribosomal RNA caused by the toxins. J Biol Chem 262:5908–5912

    CAS  PubMed  Google Scholar 

  • Ferreras JM, Barbieri L, Girbes T, Battelli MG, Rojo MA, Arias FJ, Rocher MA, Soriano F, Mendez H, Stripe F (1993) Distribution and properties of major ribosome-inactivating proteins (28S rRNA N glycosidases) of the plant Saponaria officinalis L. (Caryophyllaceae). Biochem Biophys Acta 1216:31–42

    CAS  PubMed  Google Scholar 

  • Gessner SL, Irvin JD (1980) Inhibition of elongation factor 2-dependent translocation by the pokeweed antiviral protein and ricin. J Biol Chem 255:3251–3253

    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 L. J Plant Biochem Biotech 13:13–18

    CAS  Google Scholar 

  • Gholizadeh A, Kohnehrouz BB, Santha IM, Lodha ML, Kapoor HC (2005) Cloning and expression of small cDNA fragment encoding strong antiviral peptide from Celosia cristata in E.coli. Biochemistry (Moscow) 70:1005–1010

    CAS  Google Scholar 

  • Gholizadeh A, Santha IM, Kohnehrouz BB, Lodha ML, Kapoor HC (2005) Cystatins may confer viral resistance in plants by inhibition of a virus-induced cell death phenomenon in which cysteine proteinases are active: cloning and molecular characterization of a cDNA encoding cysteine-proteinase inhibitor (celostatin) from Celosia cristata (crested cock’s comb). Biotechnol Appl Biochem 42:197–204

    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 39:10491058

    Google Scholar 

  • Grasso S, Shepherd RJ (1978) Isolation and partial characterization of virus inhibitors from plant species taxonomically related to Phytolacca. Phytopathology 68:199–205

    CAS  Google Scholar 

  • Greene AE, Allison RF (1994) Recombination between viral RNA transgenic plant transcripts. Science 263:1423–1435

    CAS  PubMed  Google Scholar 

  • Grela P, Szajwaj M, Horbowicz-Drożdżal P, Tchórzewski M (2019) How ricin damages the ribosome. Toxins (Basel) 11:241

    CAS  Google Scholar 

  • GuoYong J, Demin J, Man Li W, Guo B, Bin W, Jin DM, Weng ML, Guo BT, Wang B (1999) Transformation and expression of trichosanthin gene in tomato. Acta Bot Sin 41:334–336

    Google Scholar 

  • Hamshou M, Shang C, Zaeytijd JD, VanDamme EJM, Smagghe G (2017) Expression of ribosome-inactivating proteins from apple in tobacco plants results in enhanced resistance to Spodopteraexigua. J Asia Pac Entomol 20:1–5

    Google Scholar 

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

    CAS  Google Scholar 

  • Hartog MTD, Lubelli C, Boon L, Heerkins S, BuIjsee APO, Boer M, Stripe F (2002) Cloning and expression of cDNA coding for bouganin: a type-I ribosome inactivating protein from Bougainvillea spectabilis Willd. Eur J Biochem 269:1772–1779

    Google Scholar 

  • Hassan Y, Ogg S, Ge H (2018) Expression of novel fusion antiviral proteins ricin a chain-pokeweed antiviral protein (RTA-PAPs) in Escherichiacoli and their inhibition of protein synthesis and of hepatitis B virus in vitro. BMC Biotechnol 18:47

    PubMed  PubMed Central  Google Scholar 

  • Hause B, Nieden UZ, Lehmann J, Wasternack C, Parthier B (1994) Intracellular localization of jasmonate-induced proteins in barley leaves. Bot Acta 107(333):341

    Google Scholar 

  • He WJ, Liu WY (2004) Both N- and C-terminal regions are essential for cinnamomin A-chain to deadenylate ribosomal RNA and supercoiled double-strand DNA. Biochem J 377:17–23

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hudak KA, Bauman JD, Tumer NE (2002) Pokeweed antiviral protein binds to the cap structure of eukaryotic mRNA and depurinates the mRNA downstream of the cap. RNA 8:1148–1159

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hudak KA, Parikh BA, Di R, Baricevic M, Santana M, Seskar M, Tumer NE (2004) Generation of pokeweed antiviral protein mutations in Saccharomyces cerevisiae: evidence that ribosome depurination is not sufficient for cytotoxicity. Nucleic Acids Res 32:4244–4256

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Iglesias R, Perez Y, Torre C, Ferreras JM, Antolin P, Jimenez P, Rojo MA, Mendez E, Girbes 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

    CAS  PubMed  Google Scholar 

  • Irvin JD (1983) Pokeweed antiviral protein. Pharm Ther 21:371–387

    CAS  Google Scholar 

  • Irvin JD (1995) Antiviral proteins from phytolacca. In: Chessin M, De Borde D, Zipf A (eds) Antiviral Proteins from higher plants. CRC Press, Boca Raton, pp 65–69

    Google Scholar 

  • Irvin JD (1975) Purification and partial characterization of the antiviral protein from Phytolacca americana which inhibits eukaryotic protein synthesis. Arch Biochem Biophys 169:522–528

    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 Biophy 200:418–425

    CAS  Google Scholar 

  • Kawade K, Ishizaki T, Masud K (2008) Differential expression of ribosome-inactivating protein genes during somatic embryogenesis in spinach (Spinacia oleracea). Physiol Plant 134:270–281

    CAS  PubMed  Google Scholar 

  • Kataoka J, Habuka N, Furuno M, Miyano M, Takanami Y, Koiwai A (1991) DNA sequence of Mirabilis antiviral protein (MAP) a ribosome-inactivating protein with an antiviral property from Mirabilis jalapa L. its expression in Escherichia coli. J Biol Chem 266(13):8426–8430

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Kumar D, Hridya N, Verma NT, Krishna KT (1997) Cloning and characterization of a gene encoding an antiviral protein from Clerodendrum acculeatum L. Plant Mol Biol 33:745–751

    CAS  PubMed  Google Scholar 

  • Kumon K, Sasaki J, Sejima M, Takeuchi Y, Hayashi Y (1990) Interactions between TMV, pokeweed antiviral protein, and tobacco cell wall. Phytopathology 80:636–641

    CAS  Google Scholar 

  • Kwon YS, An CS, Liu JR, Peak K (1997) A ribosome inactivating protein from Amaranthus viridis. Biosci Biotechnol Biochem 61:1613–1614

    CAS  PubMed  Google Scholar 

  • Kwon YS, Chung SA, Jang RL, Sang SK, Haeng SL, Jeong KK, Kyung HP (2000) Molecular cloning of a cDNA encoding ribosome-inactivating protein from Amaranthus viridis and its expression in E. coli. Mol Cells 10:8–12

    CAS  PubMed  Google Scholar 

  • Legname G, Gromo G, Lord JM, Monzini N, Modena D (1993) Expression and activity of pre-dianthin 30 and dianthin 30. Biochem Biophys Res Commun 192(3):1230–1237

    CAS  PubMed  Google Scholar 

  • Li MX, Yeung HW, Pan LP, Chan SI (1991) Trichosanthin a potent HIV-1 inhibitor can cleave supercoiled DNA in vitro. Nucleic Acid Res 19:6309–6312

    CAS  PubMed  Google Scholar 

  • Ling J, Liu W, Wang TP (1994) Cleavage of supercoiled double-stranded DNA by several ribosome-inactivating proteins in vitro. FEBS Lett 345:143–146

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lodha ML, Choudhary N, Mahapatro GK, Singh B, Gupta GP (2011) Purification and evaluation of antiviral proteins from Bougainvillea xbuttiana against Helicoverpa armigera. Indian J Agric Sci 81:74–78

    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

    CAS  Google Scholar 

  • Lomonossoff GP (2015) Pathogen-derived resistance to plant viruses. Annu Rev Phytopathol 33:323–343

    Google Scholar 

  • Masayuki F, Takeshi K, Satoshi-TO TO (2001) Purification and partial characterization of figaren and RNase-like novel anti-viral protein from Cucumis figaren. J Gen Plant Pathol 67:152–158

    Google Scholar 

  • May KL, Yan Q, Tumer NE (2013) Targeting ricin to the ribosome. Toxicon 69:143–151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meng Y, Lin S, Liu SF, Fan X, Li GR, Meng YF (2014) A novel method for simultaneous production of two ribosome-inactivating proteins a-MMC and MAP30 from Momordica charantia L. PLoS One 9:e101998

    PubMed  PubMed Central  Google Scholar 

  • Mishra V, Sharma RS, Yadav S, Babu CR, Singh TP (2004) Purification and characterization of four isoforms of Himalayan mistletoe ribosome-inactivating protein from Viscum album having unique sugar affinity. Arch Biochem Biophy 423:288–301

    CAS  Google Scholar 

  • Mock JW, Ng TB, Wong RN, Yao QZ, Yeung HW, Fong WP (1996) Demonstration of ribonuclease activity in the plant ribosome-inactivating proteins alpha-and beta-Momorcharins. Life Sci 59:1853–1859

    CAS  PubMed  Google Scholar 

  • Monzingo AF, Collins EJ, Ernst SR, Irvin JD, Robertus JD (1993) The 25 A structure of pokeweed antiviral protein. J Mol Biol 233:705–715

    CAS  PubMed  Google Scholar 

  • Narayanan S, Surendranath K, Bora N, Surolia A, Kare AA (2005) Ribosome inactivating proteins and apoptosis. FEBS Lett 579:1324–1331

    CAS  PubMed  Google Scholar 

  • Narwal S, Balasubrahmanyam A, Lodha ML, Kapoor HC (2001) 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 (2001) 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 

  • Nielsen K, Boston RS (2001) Ribosome-inactivating proteins: a plant perspective. Annu Rev Plant Physiol Plant Mol Biol 52:785–816

    CAS  PubMed  Google Scholar 

  • Noronha B, Gil VL, Vincente M (1980) Occurrence of plant virus inhibitors in species of Caryophyllales I. Alternaanthera ficoidea, Amaranthus deflexus, Bougainvillea spectabilis, Chenopodium ambrosoides and Mirabilis jalapa. Arg Inst Biol Sacpaulo 47:71–76

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Parikh BA, Coetzer C, Tumer NE (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 α-Sarcin/Ricin loop of rRNA. J Biol Chem 277:41428–41437

    CAS  PubMed  Google Scholar 

  • Park SW, Kim JY, Lee JK, Hwang I, Cheong H, Nah JW (2009) Antifungal mechanism of a novel antifungal protein from pumpkin rinds against various fungal pathogens. J Agric Food Chem 57:9299–9304

    CAS  PubMed  Google Scholar 

  • Park SW, Vepachedu R, Owens RA, Vivanco JM (2004) The N-glycosidase activity of the ribosome-inactivating protein ME1 target single-stranded region of nucleic acids independent of sequence or structural motifis. J Biol Chem 279:34165–34174

    CAS  PubMed  Google Scholar 

  • Park JS, Hwang DJ, Lee SM, Kim YT, Choi SB, Cho KJ (2004) Ribosome-inactivating activity and cDNA cloning of antiviral protein isoforms of Chenopodium album. Mol Cells 17:73–80

    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

    CAS  PubMed  Google Scholar 

  • Polito L, Bortolotti M, Battelli MG, Calafato G, Bolognesi A (2019) Ricin: an ancient story for a timeless plant toxin. Toxins (Basel) 11:324–340

    CAS  Google Scholar 

  • Poyet JL, Hoeveler A (1997) Presence of an intron in a gene of PAP II the ribosome-inactivating protein from summer leaves of Phytolacca americana. Ann Bot 80:685–688

    CAS  Google Scholar 

  • Prasad V, Mishra SK, Sivastava 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

    CAS  PubMed  Google Scholar 

  • Prestle J, Schonfelder M, Adam G, Mundry KW (1992) Type-I ribosome-inactivating proteins depurinate plant 25S rRNA without species specificity. Nucleic Acids Res 20:3179–3182

    CAS  PubMed  PubMed Central  Google Scholar 

  • Przydacz M, Jones R, Pennington HG, Belmans G, Bruderer M, Greenhill R, Salter T, Wellham PAD, Cota E, Spanu PD (2020) Mode of action of the catalytic site in the N-terminal ribosome-inactivating domain of JIP60. Plant Physiol 183:385–398

    CAS  PubMed  Google Scholar 

  • Puri M, Kaur I, Kanwar RK, Gupta RC, Chauhan A, Kanwar JR (2009) Ribosome inactivating proteins (RIPs) from Momordica charantia for antiviral therapy. Curr Mol Med 9:1080–1094

    CAS  PubMed  Google Scholar 

  • Puri M, Kaur I, Perugini MA, Gupta RC (2012) Ribosome-inactivating proteins: current status and biomedical applications. Drug Discov Today 17:774–783

    CAS  PubMed  Google Scholar 

  • Qian Q, Huang L, Yi R, Wang SZ, Ding Y (2014) Enhanced resistance to blast fungus in rice (Oryza sativa L.) by expressing the ribosome-inactivating protein alpha-momorcharin. Plant Sci 217–218:1–7

    PubMed  Google Scholar 

  • Rajamohan F, Kurinov IV, Venkatachalam JK, Ukun FN (1999) Deguanylation of human immuno deficiency virus (HIV)-1 RNA by recombinant pokeweed antiviral protein. Biochem Biophys Res Commun 263:419–424

    CAS  PubMed  Google Scholar 

  • Rajamohan F, Venkatachalam TK, Irvin JD, Uckun FN (1999) Pokeweed antiviral protein isoforms PAPI PAPII and PAPIII depurinate RNA of human deficiency virus (HIV)-1. Biochem Biophys Res Commun 260:453–458

    CAS  PubMed  Google Scholar 

  • Rajesh S, Balasaraswathi R, Doraisamy S, Sadasivam S (2005) Synthesis and cloning of cDNA encoding an antiviral protein from the leaves of Bougainvillea spectabilis Willd (Nyctaginaceae). World J Agri Sci 1:101–104

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Reinbothe S, Reinbothe C, Lehmann J, Becker W, Apel K, Partheir B (1994) JIP60 a methyl jasmonates-induced ribosome inactivating protein involved in plant stress reactions. Proc Natl Acad Sci USA 91:7012–7016

    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

    CAS  PubMed  Google Scholar 

  • Rumiyati NAW, Sismindari-Lukitaningsih E, Yuliati T (2014) Potential of ribosome-inactivating proteins (RIPs) of Mirabilisjalapa L as an antiacne: effect on proliferation of cultured sebocyte cells its antibacterial activities against Propionibacteriumacnes and Staphylococcusepidermidis. Int J Pharm Chem 4:130–133

    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

    CAS  Google Scholar 

  • Shang C, Rougé P, VanDamme EJM (2016) Ribosome inactivating proteins from rosacea. Molecules 21:1105

    PubMed Central  Google Scholar 

  • Shahidi-Noghabi S, VanDamme EJM, Mahdian K, Smagghe G (2010) Entomotoxic action of Sambucus nigra agglutinin I in Acyrthosiphon pisum aphids, Spodoptera exigua caterpillars through caspase-3 like dependent apoptosis. Arch Insect Biochem Physiol 75:207–220

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Shahidi-Noghabi S, VanDamme 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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi WW, Mak AN, Wong KB, Shaw PC (2016) Structures and ribosomal interaction of ribosome-inactivating proteins. Molecules 21:1588

    PubMed Central  Google Scholar 

  • Sikriwal D, Batra JK (2010) Ribosome inactivating proteins and apoptosis. In: Lord JM, Hartley MR (eds) Plant cell monographs: toxic plant proteins. Springer, Berlin, pp 107–132

    Google Scholar 

  • Singh S (2018) A review-structure-function studies of abrin: a ribosome inactivation toxin. FASEB J 32:40 (Abstract in Experimental Biology S6852 April 21–25 2018—San Diego California)

    Google Scholar 

  • Sipahioglu HM, Kaya I, Usta M, Unal M, Ozcan D, Dilmen MO, Guller A, Pallas 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

    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

    CAS  PubMed  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

    CAS  Google Scholar 

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

    Google Scholar 

  • Thomas TMG, Yeung HW, Fong WP (1992) Deoxyribonucleolytic activity of α and β-momorcharins. Life Sci 51:1347–1353

    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 (2015) Introduction to the toxins special issue on plant toxins. Toxins (Basel) 7:4503–4506

    CAS  Google Scholar 

  • Tumer NE, Hwang D, 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

    CAS  PubMed  Google Scholar 

  • Umamaheswari RS, Nuni A (2008) In vitro antibacterial activity of Bougainvillea spectabilis leaves extracts. Adv Biol Res 2:01–05

    Google Scholar 

  • VanDamme EJM, Hao Q, Chen Y, Barre A, Venbussche F, Desmyter S, Rouge P, Peumans WJ (2001) Ribosome-inactivating proteins: a family of plant proteins that do more than inactivate ribosomes. Crit Rev Plant Sci 20:395–465

    CAS  Google Scholar 

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

    Google Scholar 

  • Vepachedu R, Bais HP, Vivanco JM (2003) Molecular characterization post-transcriptional regulation of ME1 a type-I ribosome-inactivating protein from Mirabilisexpansa. Planta 217(3):498–506

    CAS  PubMed  Google Scholar 

  • Verma HN, Awasthi LP (1980) Occurrence of highly antiviral agent in plants treated with Boerhaavia diffusa inhibitor. Can J Bot 58:2141–2144

    Google Scholar 

  • Verma HN, Baranwal VK (1983) Antiviral activity and the physical properties of the leaf extract of Chenopodiumambrosoides. Proc Indian Acad Sci (Plant Sci) 92:461–465

    Google Scholar 

  • Verma HN, Varsha BVK (1995) Agricultural role of endogenous antiviral substances of plant origin. In: Chessin M, DeBorde D, Zipf A (eds) Antiviral proteins in higher plants. CRC Press, Boca Raton, pp 23–37

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Hudak KA (2006) A novel interaction of pokeweed antiviral protein with translation initiation factors 4G and iso4G: a potential indirect mechanism to access viral RNAs. Nucleic Acids Res 34:1174–1181

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang P, Tumer NE (1999) Pokeweed antiviral protein cleaves double stranded supercoiled DNA using the same active site required to depurinate rRNA. Nucl Acids Res 27:1900–1905

    CAS  PubMed  Google Scholar 

  • Wang P, Zubenko 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

    CAS  PubMed  Google Scholar 

  • Wang S, Zhang H, Zheng Y, Li Z, Xiang F, Ding Y, Xiang J (2016) Environmental factors and phytohormones enhancing expression of a-momorcharin gene in Momordica charantia. Biologia 71:155–160

    CAS  Google Scholar 

  • Wu TH, Chow LP, Lin JY (1998) Sechiumin a ribosome-inactivating protein from the edible gourd Sechium edule Swartz–purification characterization molecular cloning and expression. Eur J Biochem 255:400–408

    CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  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

    PubMed  PubMed Central  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

    CAS  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

    CAS  PubMed  Google Scholar 

  • Zoubenko O, Hudak K, Timer 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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

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Choudhary, N., Lodha, M.L. & Baranwal, V.K. The role of enzymatic activities of antiviral proteins from plants for action against plant pathogens. 3 Biotech 10, 505 (2020). https://doi.org/10.1007/s13205-020-02495-9

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