Skip to main content

Advertisement

Log in

Purification of an antiviral protein from the seeds of quinoa (Chenopodium quinoa Willd.) and characterization of its antiviral properties

  • Original Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

Plant viral pathogens cause damaging diseases in many agriculture systems, and emerging viral infections are a serious threat for providing adequate food to a continuously growing population. Recent studies of biogenic substances have provided new opportunities for producing novel antiviral agents. The present work has been conducted to evaluate the antiviral activity of quinoa (Chenopodium quinoa Willd.) seeds crude extract. The antiviral activity was retained in different buffer solutions of various pH ranges (5.2–8.5) and remained after the diafiltration process. The putative virus inhibitor was sensitive to treatment with sodium dodecyl sulfate and trichloroacetic acid. An antiviral protein with ~ 25 kDa molecular weight was isolated from the seed quinoa extract using ammonium sulfate precipitation, anion and cation exchange chromatography. The purified protein (Quinoin-I) significantly inhibited TMV on tobacco leaves with an IC50 value at a 6.81 μg/ml concentration. Enzyme activity assay revealed the RNase activity of Quinoin-I, and this feature was retained in the presence of β-mercaptoethanol and ethylene diamine tetraacetic acid. This antiviral protein has been shown as a promising leading molecule for further development as a novel antiviral agent.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are not publicly available but are available from the corresponding author on reasonable request.

References

  • 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  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

    Article  CAS  Google Scholar 

  • Behjatnia SAA, Jahanbin D, Izadpanah K, Moghadam A (2017) Interaction of viruses causing beet curly top disease with Tomato yellow leaf curl virus in tomato plants under greenhouse conditions. Iran J Plant Pathol 53:417–430

    Google Scholar 

  • Biniaz Y, Kavoosi G, Afsharifar A (2021) Antiviral activity and tobacco-induced resistance, mediated by essential oil nano-emulsions from Zataria multiflora and Satureja bakhtiarica. Int J Pest Manag. https://doi.org/10.1080/09670874.2021.1985653

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    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(3):125–130

    CAS  Google Scholar 

  • Choudhary NL, Yadav OP, Lodha ML (2008) 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 10:1–13

    Article  Google Scholar 

  • Clark MF, Adams AN (1977) Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. J Gen Virol 34:475–483

    Article  CAS  Google Scholar 

  • Cordeiro LM, de Fátima RV, Baggio CH, de Paula Werner MF et al (2012) Arabinan and arabinan-rich pectic polysaccharides from quinoa (Chenopodium quinoa) seeds: structure and gastroprotective activity. Food Chem 130:937–944

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Duarte LML, Alexandre MAV, Noronha AB, Vicente M (1990) Behaviour of tobacco plants, singly and doubly infected by potato virus X and potato virus Y necrotic strain, in the presence of some natural inhibitors. Microbios Lett 45(179–180):131–137

    Google Scholar 

  • Dutt S, Narwal S, Kapoor HC, Lodha ML (2003a) 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, Narwal S, Kapoor HC, Lodha ML (2003b) Possible mechanism of action of antiviral proteins from the leaves of Chenopodium album L. Indian J Biochem Biophys 41(1):29–33

    Google Scholar 

  • Elena SF, Fraile A, García-Arenal F (2014) Evolution and emergence of plant viruses. Adv Virus Res 88:161–191

    Article  Google Scholar 

  • Fraenkel-Conrat H (1957) Degradation of tobacco mosaic virus with acetic acid. Virology 4:1–4

    Article  CAS  Google Scholar 

  • Francki RIB (1964) Inhibition of cucumber mosaic virus infectivity by leaf extracts. Virology 24(2):193–199

    Article  CAS  Google Scholar 

  • Fujiwara M, Kanamori T, Satoshi TO, Osaki T (2001) Purification and partial characterization of Figaren, an RNase-like novel antiviral protein from Cucumis figarei. J Gen Plant Pathol 67:152–158

    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  Google Scholar 

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

    Google Scholar 

  • Hammond J, Lawson RH (1988) An improved purification procedure for preparing potyviruses and cytoplasmic inclusions from the same tissue. J Virol Methods 20:203–217

    Article  CAS  Google Scholar 

  • Heo KJ, Kwon SJ, Kim MK, Kwak HR et al (2020) Newly emerged resistance-breaking variants of cucumber mosaic virus represent ongoing host-interactive evolution of an RNA virus. Virus Evol 6:veaa070

    Article  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  Google Scholar 

  • Ilinskaya O, Mahmud RS (2014) Ribonucleases as antiviral agents. Mol Biol 48:615–623

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Kim SG, Kim ST, Wang Y, Yu S et al (2011) The RNase activity of rice probenazole-induced protein1 (PBZ1) plays a key role in cell death in plants. Mol Cells 31:25–31

    Article  CAS  Google Scholar 

  • Kubo S, Ikeda T, Imaizumi S, Takanami Y, Mikami Y (1990) A potent plant virus inhibitor found in Mirabilis jalapa L. Jpn J Phytopathol 56:481–487

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Landi N, Ruocco MR, Ragucci S, Aliotta F et al (2021) Quinoa as source of type 1 ribosome inactivating proteins: a novel knowledge for a revision of its consumption. Food Chem 342:128337

    Article  CAS  Google Scholar 

  • McLeish MJ, Fraile A, García-Arenal F (2020) Trends and gaps in forecasting plant virus disease risk. Ann Appl Biol 176:102–108

    Article  Google Scholar 

  • Musidlak O, Nawrot R, Goździcka-Józefiak A (2017) Which plant proteins are involved in antiviral defense? Review on in vivo and in vitro activities of selected plant proteins against viruses. Int J Mol Sci 18:2300

    Article  Google Scholar 

  • Nelson R (2020) International plant pathology: past and future contributions to global food security. Phytopathology 110:245–253

    Article  Google Scholar 

  • Nicaise V (2014) Crop immunity against viruses: outcomes and future challenges. Front Plant Sci 5:660

    Article  Google Scholar 

  • Park YJ, Moon C, Kang JH, Choi TJ (2017) Antiviral effects of extracts from Celosia cristata and Raphanus sativus roots against viral hemorrhagic septicemia virus. Adv Virol 162:1711–1716

    CAS  Google Scholar 

  • Pizzo E, Di Maro A (2016) A new age for biomedical applications of Ribosome Inactivating Proteins (RIPs): from bioconjugate to nanoconstructs. J Biomed Sci 23:1–8

    Article  Google Scholar 

  • Rasoulpour R, Afsharifar A, Izadpanah K, Aminlari M (2017) Purification and characterization of an antiviral protein from prickly pear (Opuntia ficus-indica (L.) Miller) cladode. Crop Prot 93:33–42

    Article  CAS  Google Scholar 

  • Rasoulpour R, Afsharifar A, Izadpanah K (2018) Antiviral activity of prickly pear (Opuntia ficus-indica (L.) Miller) extract: Opuntin B, a second antiviral protein. Crop Prot 112:1–9

    Article  CAS  Google Scholar 

  • Rasoulpour R, Izadpanah K, Afsharifar A (2020) Opuntin B, the antiviral protein isolated from prickly pear (Opuntia ficus-indica (L.) Miller) cladode exhibits ribonuclease activity. Microb Pathog 140:103929

    Article  CAS  Google Scholar 

  • Ray B, Schütz M, Mukherjee S, Jana S et al (2021) Exploiting the amazing diversity of natural source-derived polysaccharides: modern procedures of isolation, engineering, and optimization of antiviral activities. Polymers 13:136

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Saksena K, Mink G (1969) Properties of an inhibitor of apple chlorotic leaf spot virus from Chenopodium quinoa. Phytopathology 59:63

    Google Scholar 

  • Scott H (1963) Purification of cucumber mosaic virus. Virology 20:103–106

    Article  CAS  Google Scholar 

  • Sezgin AC, Sanlier N (2019) A new generation plant for the conventional cuisine: Quinoa (Chenopodium quinoa Willd.). Trends Food Sci Technol 86:51–58

    Article  Google Scholar 

  • Soleimani R, Matic S, Taheri H, Behjatnia SAA et al (2013) The unconventional geminivirus beet curly top Iran virus: satisfying Koch’s postulates and determining vector and host range. Ann Appl Biol 162:174–181

    Article  CAS  Google Scholar 

  • Song SK, Choi Y, Moon YH, Kim SG et al (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  Google Scholar 

  • Taniguchi T, Goto T (1976) Purification of an inhibitor of plant virus infection occurring in the leaves of Chenopodium amaranticolor. Jpn J Phytopathol 42:42–45

    Article  Google Scholar 

  • Thomson AD, Peddie BA (1965) Studies on a virus inhibitor from Chenopodium leaves. NZ J Agric Res 8(4):825–831

    Article  Google Scholar 

  • Verma H, Baranwal V (1983) Antiviral activity and the physical properties of the leaf extract of Chenopodium ambrosoides L. Proc Plant Sci 92:461–465

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Vilcacundo R, Hernández-Ledesma B (2017) Nutritional and biological value of quinoa (Chenopodium quinoa Willd.). Curr Opin Food Sci 14:1–6

    Article  Google Scholar 

  • Yang F, Wei NN, Gao R, Piao XC, Lian ML (2015) Effect of several medium factors on polysaccharide and alkaloid accumulation in protocorm-like bodies of Dendrobium candidum during bioreactor culture. Acta Physiol Plant 37:94

    Article  Google Scholar 

  • Zhao L, Feng C, Wu K, Chen W et al (2017) Advances and prospects in biogenic substances against plant virus: a review. Pestic Biochem Physiol 135:15–26

    Article  CAS  Google Scholar 

  • Zhu F, Yuan S, Zhang ZW, Qian K et al (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 

Download references

Acknowledgements

We sincerely thank Dr. Nasrin Kazemipour from the Biochemistry Division, School of Veterinary Medicine, Shiraz University for their generous laboratory support.

Funding

This research was funded by Shiraz University.

Author information

Authors and Affiliations

Authors

Contributions

YB; methodology, YB; formal analysis, MK; validation, YB, MK; investigation, YB; writing–original draft preparation, MK, AN, AA; reviewed and edited the manuscript, AA; supervision, AA; project administration. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Alireza Afsharifar.

Ethics declarations

Competing interests

The authors declare no competing interests.

Conflict of interest

The authors declare that they have no conflict of interest in the publication.

Ethical approval and consent to participate

The study was granted exemption from requiring ethics approval because human participants, their data or biological material were not involved.

Additional information

Handling editor: M. Bromke.

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

Biniaz, Y., Khalesi, M., Niazi, A. et al. Purification of an antiviral protein from the seeds of quinoa (Chenopodium quinoa Willd.) and characterization of its antiviral properties. Amino Acids 55, 19–31 (2023). https://doi.org/10.1007/s00726-022-03200-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-022-03200-1

Keywords

Navigation