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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

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Abstract

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Two virus inhibitory proteins were purified from Cyamopsis tetragonoloba , induced to resist virus infections by CIP-29, a systemic resistance inducing protein from Clerodendrum inerme , and characterized. One of them shared homology with a lectin.

Abstract

CIP-29, a known 29 kDa systemic antiviral resistance inducing protein isolated from Clerodendrum inerme, has been used to induce systemic resistance in Cyamopsis tetragonoloba against Sunn-hemp rosette virus (SRV). Paper reports the detection of virus inhibitory activity in induced-resistant leaf sap of C. tetragonoloba, and the purification of two virus inhibitory agents (VIAs) thereof. VIA activity was recorded as a reduction in lesion number of SRV, Tobacco mosaic virus, and Papaya ringspot virus, when they were incubated separately with resistant sap and inoculated onto susceptible C. tetragonoloba, Nicotiana tabacum cv. Xanthi-nc, and Chenopodium quinoa, respectively. The two VIAs were isolated from resistant C. tetragonoloba plant leaves using combinations of column chromatography. Both were basic proteins, and since their M r was 32 and 62 kDa, these VIAs were called CT-VIA-32 and CT-VIA-62, respectively, on the basis of their molecular mass and the host. CT-VIA-62 displayed better activity, and was thus studied further. It tested positive for a glycoprotein, and was serologically detected only in leaf tissue post-induction. Tryptic peptides generated in-gel, post SDS-PAGE of CT-VIA-62, were sequenced through LC/MS/MS. All CT-VIA-62 peptides were found to share homologies with proteins from Medicago truncatula that possess a mannose-binding lectin domain.

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Abbreviations

AVF:

Antiviral factor

CAP-34:

34 kDa Systemic antiviral resistance inducing protein from Clerodendrum aculeatum

CIP-29:

29 kDa Systemic antiviral resistance inducing protein from Clerodendrum inerme

ISR:

Induced systemic resistance

IVR:

Inhibitor of virus replication

PGPR:

Plant growth promoting rhizobacteria

PR-protein:

Pathogenesis-related protein

PRSV:

Papaya ringspot virus

RIP:

Ribosome inactivating protein

SAR:

Systemic acquired resistance

SDS-PAGE:

Sodium dodecyl sulfate-polyacrylamide gel electrophoresis

SRV:

Sunn-hemp rosette virus

TMV:

Tobacco mosaic virus

VIA:

Virus inhibitory agent

References

  • Akad F, Teverovsky E, David A, Czosnek H, Gidoni D, Gera A, Loebenstein G (1999) A cDNA from tobacco codes for an inhibitor of virus replication(IVR)-like protein. Plant Mol Biol 40:969–976

    Article  CAS  PubMed  Google Scholar 

  • Akad F, Teverovsky E, Gidoni D, Elad Y, Kirshner B, Rav-David D, Czosnek H, Loebenstein G (2005) Resistance to Tobacco mosaic virus and Botrytis cinerea in tobacco transformed with complementary DNA encoding an inhibitor of virus replication-like protein. Ann Appl Biol 147:89–100

    Article  CAS  Google Scholar 

  • Antoniw JF, White RF (1980) The effects of aspirin and polyacrylic acid on soluble leaf proteins and resistance to virus infection in five cultivars of tobacco. Phytopath Z 98:331–341

    Article  CAS  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 Central  PubMed  Google Scholar 

  • Cadman E, Bostwick JR, Eichberg J (1979) Determination of protein by modified Lowry procedure in the presence of some commonly used detergents. Anal Biochem 96:21–23

    Article  CAS  PubMed  Google Scholar 

  • Chisholm ST, Mahajan SK, Whitham SA, Yamamoto ML, Carrington JC (2000) Cloning of the Arabidopsis RTM1 gene, which controls restriction of long-distance movement of tobacco etch virus. Proc Nat Acad Sci USA 97:489–494

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dann EK, Diers B, Byrum J, Hammerschmidt R (1998) Effect of treating soybean with 2,6-dichloro-isonicotinic acid (INA) and benzothiadiazole (BTH) on seed yields and the level of disease caused by Sclerotinia sclerotiorum in field and greenhouse studies. Eur J Pl Path 104:271–278

    Article  CAS  Google Scholar 

  • De Hoff PL, Brill LM, Hirsch AM (2009) Plant lectins: the ties that bind in root symbiosis and plant defense. Mol Genet Gen 282:1–15

    Article  Google Scholar 

  • Edelbaum O, Ilan N, Grafi G, Sher N, Stram Y, Novick D, Tal N, Sela I, Rubinstein M (1990) Two antiviral proteins from tobacco: purification and characterization by monoclonal antibodies to human β-interferon. Proc Nat Acad of Sci USA 87:588–592

    Article  CAS  Google Scholar 

  • Edelbaum O, Sher N, Rubinstein M, Novick D, Tal N, Moyer M, Ward E, Ryals J, Sela I (1991) Two antiviral proteins, gp35 and gp22 correspond to 1,3-β-glucanase and an isoform of PR-5. Plant Mol Biol 17:171–173

    Article  CAS  PubMed  Google Scholar 

  • Elad Y, Rav-David D, Leibman D, Vintal H, Vunsh R, Moorthy H, Gal-On A, Loebenstein G (2012) Tomato plants transformed with the inhibitor-of-virus-replication gene are partially resistant to several pathogenic fungi. Ann Appl Biol 161:16–23

    Article  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 characteristics of the modification in 28S ribosomal RNA caused by the toxins. J Biol Chem 262:5908–5912

    CAS  PubMed  Google Scholar 

  • Friedrich L, Lawton K, Ruess W, Masner P, Specker N, GutRella MB, Dincher S, Staub T, Uknes S, Metraux J-P, Kessmann H, Ryals J (1996) A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J 10:61–70

    Article  CAS  Google Scholar 

  • Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Ann Rev Plant Biol 64:839–863

    Article  CAS  Google Scholar 

  • Gera A, Loebenstein G (1983) Further studies of an inhibitor of virus replication from TMV infected protoplast of a local lesion responding tobacco cultivar. Phytopathology 73:111–115

    Article  Google Scholar 

  • Gera A, Loebenstein G, Salomon R, Franck A (1990) Inhibitor of virus replication (IVR) from protoplast of a hypersensitive tobacco cultivar infected with tobacco mosaic virus is associated with a 23 k protein species. Phytopathology 80:78–81

    Article  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  PubMed  Google Scholar 

  • Gonsalves D, Ishii M (1980) Purification and serology of papaya ringspot virus. Phytopathology 70:1028–1032

    Article  CAS  Google Scholar 

  • Gooding GV, Hebert TT (1967) A simple technique for purification of tobacco mosaic virus in large quantities. Phytopathology 57:1285

    PubMed  Google Scholar 

  • Hwang IS, Hwang BK (2011) The pepper mannose-binding lectin gene CaMBL1 is required to regulate cell death and defense responses to microbial pathogens. Pl Physiol 155:447–463

    Article  CAS  Google Scholar 

  • Kumar D, Verma HN, Tuteja N, Tewari KK (1997) Cloning and characterization of a gene encoding an antiviral protein from Clerodendrum aculeatum L. Pl Mol Biol 33:745–751

    Article  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Loebenstein G, Gera A (1981) Inhibitor of virus replication released from TMV infected protoplasts of a local lesion responding tobacco cultivar. Virology 114:132–139

    Article  CAS  PubMed  Google Scholar 

  • Loebenstein G, Rav-David D, Leibman D, Gal-On A, Vunsh R, Czosnek H, Elad Y (2010) Tomato plants transformed with the inhibitor-of-virus-replication gene are partially resistant to Botrytis cinerea. Phytopathology 100:225–229

    Article  CAS  PubMed  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant growth-promoting rhizobacteria. Ann Rev Microbiol 63:541–556

    Article  CAS  Google Scholar 

  • Matthieu JM, Quarles RH (1973) Quantitative scanning of glycoproteins on polyacrylamide gels stained with periodic acid-schiff reagent (PAS). Anal Biochem 55:313–316

    Article  CAS  PubMed  Google Scholar 

  • Mozes R, Antignus Y, Sela I, Harpaz I (1978) The chemical nature of an antiviral factor (AVF) from virus-infected plants. J Gen Virol 38:241–249

    Article  CAS  Google Scholar 

  • Neumann U, Khalaf H, Rimpler M (1994) Quantification of electrophoretically separated proteins in the submicrogram range by dye elution. Electrophoresis 15:916–921

    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 Lett 396:132–134

    Article  CAS  PubMed  Google Scholar 

  • Peumans WJ, Van Damme EJM (1995) Lectins as plant defense proteins. Pl Physiol 109:347–352

    Article  CAS  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, Misra SK, Krishna SK (2012) Induced systemic resistance against viruses in susceptible plants: phytoproteins and rhizobacteria provide two fascinating avenues. In: Rao GP, Baranwal VK, Mandal B, Rishi N (eds) Recent trends in plant virology. Studium Press LLC, Houston, pp 467–482

    Google Scholar 

  • Ross AF (1961) Systemic acquired resistance induced to localized virus infections in plants. Virology 14:340–358

    Article  CAS  PubMed  Google Scholar 

  • Sela I, Applebaum SW (1962) Occurrence of an antiviral factor in virus infected plants. Virology 17:543–548

    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 Pl Pathol 123:241–246

    Article  CAS  Google Scholar 

  • Stevens WA, Spurdon C, Onyon LJ, Stirpe F (1981) Effect of inhibitors of protein synthesis from plants on tobacco mosaic virus infection. Experientia 37:257–259

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Towbin H, Stahelin T, Gordon J (1979) Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Nat Acad Sci USA 76:4350–4354

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Van Damme EJM, Barre A, Rouge P, Peumans WJ (2004) Cytoplasmic/nuclear plant lectins: a new story. Trends in Pl Sci 9:484–489

    Article  Google Scholar 

  • Van Damme EJM, Lannoo N, Peumans WJ (2008) Plant lectins. Adv Bot Res 48:108–209

    Google Scholar 

  • Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Ann Rev Phytopath 36:453–483

    Article  Google Scholar 

  • Verma HN, Dwivedi SD (1984) Properties of a virus inhibiting agent isolated from plants following treatment with Bougainvillea spectabilis leaf extract. Physiol Plant Pathol 25:93–101

    Article  CAS  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 

  • Wang P, Tumer NE (2000) Virus resistance mediated by ribosome-inactivating proteins. Adv Virus Res 55:325–355

    Article  CAS  PubMed  Google Scholar 

  • Yamaji Y, Maejima K, Ozeki J, Komatsu K, Shiraishi T, Okano Y, Himeno M, Sugawara K, Neriya Y, Minato N, Miura C, Hashimoto M, Namba S (2012) Lectin-mediated resistance impairs plant virus infection at the cellular level. Pl Cell 24:778–793

    Article  CAS  Google Scholar 

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Acknowledgments

Financial assistance for this work under research project no. SP/SO/A-29/99 sanctioned by the Department of Science and Technology, Government of India, is gratefully acknowledged. Biswajeet Thakur and Manoj M. C. are thanked for the regression analysis.

Conflict of interest

The authors declare that there is no conflict of interest.

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Authors and Affiliations

  1. Molecular Plant Virology Lab, Department of Botany, Lucknow University, Lucknow, 226007, India

    Vivek Prasad, Santosh Kumar Mishra, Shalini Srivastava & Aparana Srivastava

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  1. Vivek Prasad
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  2. Santosh Kumar Mishra
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  3. Shalini Srivastava
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  4. Aparana Srivastava
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Correspondence to Vivek Prasad.

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Communicated by M. Prasad.

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Prasad, V., Mishra, S.K., Srivastava, S. et al. 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 (2014). https://doi.org/10.1007/s00299-014-1630-7

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  • DOI: https://doi.org/10.1007/s00299-014-1630-7

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