Antifungal Proteins from Plant Latex

Author(s): Mayck Silva Barbosa, Bruna da Silva Souza, Ana Clara Silva Sales, Jhoana D’arc Lopes de Sousa, Francisca Dayane Soares da Silva, Maria Gabriela Araújo Mendes, Káritta Raquel Lustoza da Costa, Taiane Maria de Oliveira, Tatiane Caroline Daboit, Jefferson Soares de Oliveira*

Journal Name: Current Protein & Peptide Science

Volume 21 , Issue 5 , 2020

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Graphical Abstract:


Latex, a milky fluid found in several plants, is widely used for many purposes, and its proteins have been investigated by researchers. Many studies have shown that latex produced by some plant species is a natural source of biologically active compounds, and many of the hydrolytic enzymes are related to health benefits. Research on the characterization and industrial and pharmaceutical utility of latex has progressed in recent years. Latex proteins are associated with plants’ defense mechanisms, against attacks by fungi. In this respect, there are several biotechnological applications of antifungal proteins. Some findings reveal that antifungal proteins inhibit fungi by interrupting the synthesis of fungal cell walls or rupturing the membrane. Moreover, both phytopathogenic and clinical fungal strains are susceptible to latex proteins. The present review describes some important features of proteins isolated from plant latex which presented in vitro antifungal activities: protein classification, function, molecular weight, isoelectric point, as well as the fungal species that are inhibited by them. We also discuss their mechanisms of action.

Keywords: Latex, proteins, plant, metabolism, antifungal agents, enzymes.

Hagel, J.M.; Yeung, E.C.; Facchini, P.J. Got milk? The secret life of laticifers. Trends Plant Sci., 2008, 13(12), 631-639.
[] [PMID: 18977166]
Pickard, W.F. Laticifers and secretory ducts: two other tube systems in plants. New Phytol., 2008, 177(4), 877-888.
[] [PMID: 18086227]
Flemmig, M.; Domsalla, A.; Rawel, H.; Melzig, M.F. Isolation and characterization of mauritanicain, a serine protease from the latex of Euphorbia mauritanica L. Planta Med., 2017, 83(6), 551-556.
[PMID: 27680709]
Santana, L.A.B.; Aragão, D.P.; Araújo, T.S.L.; Sousa, N.A.; Souza, L.K.M.; Oliveira, L.E.S.; Pereira, A.C.T.D.C.; Ferreira, G.P.; Oliveira, N.V.M.; Souza, B.D.S.; Sousa, F.B.M.; Ramos, M.V.; Freitas, C.D.T.; Medeiros, J.R.; Oliveira, J.S. Antidiarrheal effects of water-soluble proteins from Plumeria pudica latex in mice. Biomed. Pharmacother., 2018, 97, 1147-1154.
[] [PMID: 29136953]
Nawrot, R.; Józefiak, D.; Sip, A.; Kuźma, D.; Musidlak, O.; Goździcka-Józefiak, A. Isolation and characterization of a nonspecific lipid transfer protein from Chelidonium majus L. Latex. J. Biol. Macromol., 2017, 104(Pt A), 554-563.
Sharma, A.; Kumari, M.; Jagannadham, M.V. Benghalensin, a highly stable serine protease from the latex of medicinal plant Ficus benghalensis. J. Agric. Food Chem., 2009, 57(23), 11120-11126.
[] [PMID: 19886667]
Kuster, V.C.; Silva, L.C.; Meira, R.M.S.A.; Azevedo, A.A. Glandular Trichomes and Laticifers in Leaves of Ipomoea Pes-Caprae and I. Imperati (Convolvulaceae) from Coastal Restinga Formation: Structure and Histochemistry. Braz. J. Bot., 2016, 39(4), 1117-1125.
Geraci, A.; Polizzano, V.; Schicchi, R. Ethnobotanical Uses of Wild Taxa as Galactagogues in Sicily (Italy). Acta Soc. Bot. Pol., 2018, 87(2), 11-27.
Moon, J.M.; Lee, B.K.; Chun, B.J. Toxicities of raw Alocasia odora. Hum. Exp. Toxicol., 2011, 30(10), 1720-1723.
[] [PMID: 21177728]
Seigler, D.S. Phytochemistry and systematics of the euphorbiaceae. Ann. Mo. Bot. Gard., 1994, 81(2), 380-401.
Cordeiro Arruda, M.F.; Takaki Rosa, R.; Ribeiro Rosa, E.A.; Stuelp Campelo, P.M. Atividade antimicrobiana e toxicidade do látex de Euphorbia tirucalli L. (Aveloz). Rev. Cuba. Plantas Med., 2015, 20(4), 492-497.
Freitas, C.D.T.; Oliveira, J.S.; Miranda, M.R.A.; Macedo, N.M.R.; Sales, M.P.; Villas-Boas, L.A.; Ramos, M.V. Enzymatic activities and protein profile of latex from Calotropis procera. Plant Physiol. Biochem., 2007, 45(10-11), 781-789.
[] [PMID: 17888673]
Malek, K.; Norazan, M.; Ramaness, P.; Othman, Z.; Malek, R.; Aziz, R.; Aladdin, A.; El Enshasy, H. Cysteine proteases from Carica papaya: An important enzyme group of many industrial applications. IOSR J. Pharm. Biol. Sci., 2016, 11(2), 11-16.
Nürnberger, T.; Brunner, F.; Kemmerling, B.; Piater, L. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev., 2004, 198, 249-266.
[] [PMID: 15199967]
Souza, D.P.; Freitas, C.D.T.; Pereira, D.A.; Nogueira, F.C.; Silva, F.D.A.; Salas, C.E.; Ramos, M.V. Laticifer proteins play a defensive role against hemibiotrophic and necrotrophic phytopathogens. Planta, 2011, 234(1), 183-193.
[] [PMID: 21394468]
de Freitas, C.D.; Lopes, J.L. de S.; Beltramini, L.M.; de Oliveira, R.S.; Oliveira, J.T.A.; Ramos, M.V. Osmotin from Calotropis procera latex: new insights into structure and antifungal properties. Biochim. Biophys. Acta, 2011, 1808(10), 2501-2507.
[] [PMID: 21798235]
Yan, J.; Yuan, S.S.; Jiang, L.L.; Ye, X.J.; Ng, T.B.; Wu, Z.J. Plant antifungal proteins and their applications in agriculture. Appl. Microbiol. Biotechnol., 2015, 99(12), 4961-4981.
[] [PMID: 25971197]
Patel, A.K.; Singh, V.K.; Yadav, R.P.; Moir, A.J.G.; Jagannadham, M.V. ICChI, a glycosylated chitinase from the latex of Ipomoea carnea. Phytochemistry, 2009, 70(10), 1210-1216.
[] [PMID: 19683318]
Wong, J.H.; Ng, T.B. Sesquin, a potent defensin-like antimicrobial peptide from ground beans with inhibitory activities toward tumor cells and HIV-1 reverse transcriptase. Peptides, 2005, 26(7), 1120-1126.
[] [PMID: 15949629]
Lopes, J.L.S.; Valadares, N.F.; Moraes, D.I.; Rosa, J.C.; Araújo, H.S.S.; Beltramini, L.M. Physico-chemical and antifungal properties of protease inhibitors from Acacia plumosa. Phytochemistry, 2009, 70(7), 871-879.
[] [PMID: 19443001]
Ramos, M.V.; Demarco, D.; da Costa Souza, I.C.; de Freitas, C.D.T. Laticifers, latex, and their role in plant defense. Trends Plant Sci., 2019, 24(6), 553-567.
[] [PMID: 30979674]
de Freitas, C.D.; Nogueira, F.C.S.; Vasconcelos, I.M.; Oliveira, J.T.A.; Domont, G.B.; Ramos, M.V. Osmotin purified from the latex of Calotropis procera: biochemical characterization, biological activity and role in plant defense. Plant Physiol. Biochem., 2011, 49(7), 738-743.
[] [PMID: 21334906]
Selitrennikoff, C.P. Antifungal proteins. Appl. Environ. Microbiol., 2001, 67(7), 2883-2894.
[] [PMID: 11425698]
Ferreira, R.B.; Monteiro, S.; Freitas, R.; Santos, C.N.; Chen, Z.; Batista, L.M.; Duarte, J.; Borges, A.; Teixeira, A.R. The role of plant defence proteins in fungal pathogenesis. Mol. Plant Pathol., 2007, 8(5), 677-700.
[] [PMID: 20507530]
Tossi, A.; Sandri, L.; Giangaspero, A. Amphipathic, α-helical antimicrobial peptides. Biopolymers, 2000, 55(1), 4-30.
[<4:AID-BIP30>3.0.CO;2-M] [PMID: 10931439]
Theis, T.; Stahl, U. Antifungal proteins: targets, mechanisms and prospective applications. Cell. Mol. Life Sci., 2004, 61(4), 437-455.
[] [PMID: 14999404]
Ramos, M.V.; de Oliveira, R.S.; Pereira, H.M.; Moreno, F.B.M.B.; Lobo, M.D.P.; Rebelo, L.M.; Brandão-Neto, J.; de Sousa, J.S.; Monteiro-Moreira, A.C.O.; Freitas, C.D.; Grangeiro, T.B. Crystal structure of an antifungal osmotin-like protein from Calotropis procera and its effects on Fusarium solani spores, as revealed by atomic force microscopy: Insights into the mechanism of action. Phytochemistry, 2015, 119, 5-18.
[] [PMID: 26456062]
Silva, R.F. Análise histológica de tecidos cultivados in vitro de plantas laticíferas, perfil de proteínas solúveis e ação contra fitopatógenos.,. 2015.
Oliveira, H.P.; Silva, R.G.G.; Oliveira, J.T.A.; Sousa, D.O.B.; Pereira, M.L.; Souza, P.F.N.; Soares, A.A.; Gomes, V.M.; Monteiro-Moreira, A.C.O.; Moreno, F.B.M.B.; Vasconcelos, I.M. A novel peroxidase purified from Marsdenia megalantha latex inhibits phytopathogenic fungi mediated by cell membrane permeabilization. Int. J. Biol. Macromol., 2017, 96, 743-753.
[] [PMID: 28057569]
Punja, Z.K. Genetic engineering of plants to enhance resistance to fungal pathogens - a review of progress and future prospects. Can. J. Plant Pathol., 2001, 23, 216-235.
Park, S.W.; Vepachedu, R.; Sharma, N.; Vivanco, J.M. Ribosome-inactivating proteins in plant biology. Planta, 2004, 219(6), 1093-1096.
[] [PMID: 15605180]
Prasad, R.; Shah, A.H.; Rawal, M.K. Antifungals: mechanism of action and drug resistance.Yeast Membrane Transport; Ramos, J., Ed.; Springer: Cham, 2016, pp. 327-349.
Domsalla, A.; Garshasebi, A.; Melzig, M. Inhibitory Profile of Latex-Proteases in the Genus Euphorbia. Planta Med., 2008, 74(12), 699-711.
[] [PMID: 18496785]
Dubey, V.K.; Jagannadham, M.V. Procerain, a stable cysteine protease from the latex of Calotropis procera. Phytochemistry, 2003, 62(7), 1057-1071.
[] [PMID: 12591258]
Teixeira, R.D.; Ribeiro, H.A.L.; Gomes, M.T.R.; Lopes, M.T.P.; Salas, C.E. The proteolytic activities in latex from Carica candamarcensis. Plant Physiol. Biochem., 2008, 46(11), 956-961.
[] [PMID: 18672376]
Ramos, M.V.; Souza, D.P.; Gomes, M.T.R.; Freitas, C.D.T.; Carvalho, C.P.S.; Júnior, P.A.V.R.; Salas, C.E. A phytopathogenic cysteine peptidase from latex of wild rubber vine Cryptostegia grandiflora. Protein J., 2014, 33(2), 199-209.
[] [PMID: 24596120]
Siritapetawee, J.; Thammasirirak, S.; Samosornsuk, W. Antimicrobial activity of a 48-kDa protease (AMP48) from Artocarpus heterophyllus latex. Eur. Rev. Med. Pharmacol. Sci., 2012, 16(1), 132-137.
[PMID: 22338560]
Torres-Ossandón, M.J.; Vega-Gálvez, A.; Salas, C.E.; Rubio, J.; Silva-Moreno, E.; Castillo, L. Antifungal activity of proteolytic fraction (P1G10) from (Vasconcellea cundinamarcensis) latex inhibit cell growth and cell wall integrity in Botrytis cinerea. Int. J. Food Microbiol., 2019, 289, 7-16.
[] [PMID: 30193124]
Mohapatra, R.K.; Nanda, S. In silico analysis of onion chitinases using transcriptome data. Bioinformation, 2018, 14(8), 440-445.
[] [PMID: 30310251]
Kaya, M.; Baublys, V.; Šatkauskienė, I.; Akyuz, B.; Bulut, E.; Tubelytė, V. First chitin extraction from Plumatella repens (Bryozoa) with comparison to chitins of insect and fungal origin. Int. J. Biol. Macromol., 2015, 79, 126-132.
[] [PMID: 25940531]
Yeh, S.; Moffatt, B.A.; Griffith, M.; Xiong, F.; Yang, D.S.C.; Wiseman, S.B.; Sarhan, F.; Danyluk, J.; Xue, Y.Q.; Hew, C.L.; Doherty-Kirby, A.; Lajoie, G. Chitinase genes responsive to cold encode antifreeze proteins in winter cereals. Plant Physiol., 2000, 124(3), 1251-1264.
[] [PMID: 11080301]
Kesari, P.; Patil, D.N.; Kumar, P.; Tomar, S.; Sharma, A.K.; Kumar, P. Structural and functional evolution of chitinase-like proteins from plants. Proteomics, 2015, 15(10), 1693-1705.
[] [PMID: 25728311]
Ahmed, N.U.; Park, J.I.; Seo, M.S.; Kumar, T.S.; Lee, I.H.; Park, B.S.; Nou, I.S. Identification and expression analysis of chitinase genes related to biotic stress resistance in Brassica. Mol. Biol. Rep., 2012, 39(4), 3649-3657.
[] [PMID: 21720758]
Ebrahim, S.; Usha, K.; Singh, B. Pathogenesis Related (PR) Proteins in Plant Defense Mechanism. Sci Against Microb Pathog., 2011, 2, 1043-1054.
Freitas, C.D.T.; Viana, C.A.; Vasconcelos, I.M.; Moreno, F.B.B.; Lima-Filho, J.V.; Oliveira, H.D.; Moreira, R.A.; Monteiro-Moreira, A.C.O.; Ramos, M.V. First insights into the diversity and functional properties of chitinases of the latex of Calotropis procera. Plant Physiol. Biochem., 2016, 108, 361-371.
[] [PMID: 27521700]
Taira, T.; Ohdomari, A.; Nakama, N.; Shimoji, M.; Ishihara, M. Characterization and antifungal activity of gazyumaru (Ficus microcarpa) latex chitinases: both the chitin-binding and the antifungal activities of class I chitinase are reinforced with increasing ionic strength. Biosci. Biotechnol. Biochem., 2005, 69(4), 811-818.
[] [PMID: 15849422]
Kitajima, S.; Taira, T.; Oda, K.; Yamato, K.T.; Inukai, Y.; Hori, Y. Comparative study of gene expression and major proteins’ function of laticifers in lignified and unlignified organs of mulberry. Planta, 2012, 235(3), 589-601.
[] [PMID: 21993816]
Shukla, A.; Gundampati, R.K.; Jagannadham, M.V. Biochemical and Biophysical Characterization of a Peroxidase Isolated from Euphorbia tirucalli with Antifungal Activity. Biocatal. Biotransform., 2016, 34(5), 236-248.
Bolwell, G.P.; Wojtaszek, P. Mechanisms for the Generation of Reactive Oxygenspecies in Plant Defence - a Broad Perspective. Physiol. Mol. Plant Pathol., 1997, 51, 347-366.
Heller, J.; Tudzynski, P. Reactive oxygen species in phytopathogenic fungi: signaling, development, and disease. Annu. Rev. Phytopathol., 2011, 49(1), 369-390.
[] [PMID: 21568704]
Mir, A.A.; Park, S.Y.; Abu Sadat, M.; Kim, S.; Choi, J.; Jeon, J.; Lee, Y.H. Systematic characterization of the peroxidase gene family provides new insights into fungal pathogenicity in Magnaporthe oryzae. Sci. Rep., 2015, 5, 11831.
[] [PMID: 26134974]
Levine, A.; Tenhaken, R.; Dixon, R.; Lamb, C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell, 1994, 79(4), 583-593.
[] [PMID: 7954825]
Hückelhoven, R. Cell wall-associated mechanisms of disease resistance and susceptibility. Annu. Rev. Phytopathol., 2007, 45(1), 101-127.
[] [PMID: 17352660]
Dias, Rde.O.; Machado, Ldos.S.; Migliolo, L.; Franco, O.L. Insights into animal and plant lectins with antimicrobial activities. Molecules, 2015, 20(1), 519-541.
[] [PMID: 25569512]
Peumans, W.J.; Van Damme, E.J. Lectins as plant defense proteins. Plant Physiol., 1995, 109(2), 347-352.
[] [PMID: 7480335]
Datta, D.; Pohlentz, G.; Schulte, M.; Kaiser, M.; Goycoolea, F.M.; Müthing, J.; Mormann, M.; Swamy, M.J. Physico-chemical characteristics and primary structure of an affinity-purified α-D-galactose-specific, jacalin-related lectin from the latex of mulberry (Morus indica). Arch. Biochem. Biophys., 2016, 609, 59-68.
[] [PMID: 27664852]
Lam, S.K.; Ng, T.B. Lectins: production and practical applications. Appl. Microbiol. Biotechnol., 2011, 89(1), 45-55.
[] [PMID: 20890754]
da Silva, J.D.F.; da Silva, S.P.; da Silva, P.M.; Vieira, A.M.; de Araújo, L.C.C.; de Albuquerque Lima, T.; de Oliveira, A.P.S.; do Nascimento Carvalho, L.V.; da Rocha Pitta, M.G.; de Melo Rêgo, M.J.B.; Pinheiro, I.O.; Zingali, R.B.; do Socorro de Mendonça Cavalcanti, M.; Napoleão, T.H.; Paiva, P.M.G. Portulaca elatior root contains a trehalose-binding lectin with antibacterial and antifungal activities. Int. J. Biol. Macromol., 2019, 126, 291-297.
[] [PMID: 30583005]
Breitenbach Barroso Coelho, L.C.; Marcelino Dos Santos Silva, P.; Felix de Oliveira, W.; de Moura, M.C.; Viana Pontual, E.; Soares Gomes, F.; Guedes Paiva, P.M.; Napoleão, T.H.; Dos Santos Correia, M.T. Lectins as antimicrobial agents. J. Appl. Microbiol., 2018, 125(5), 1238-1252.
[] [PMID: 30053345]
Van Parijs, J.; Broekaert, W.F.; Goldstein, I.J.; Peumans, W.J. Hevein: an antifungal protein from rubber-tree (Hevea brasiliensis) latex. Planta, 1991, 183(2), 258-264.
[] [PMID: 24193629]
Berthelot, K.; Peruch, F.; Lecomte, S. Highlights on Hevea brasiliensis (pro)hevein proteins. Biochimie, 2016, 127, 258-270.
[] [PMID: 27317253]
Kanokwiroon, K.; Teanpaisan, R.; Wititsuwannakul, D.; Hooper, A.B.; Wititsuwannakul, R. Antimicrobial activity of a protein purified from the latex of Hevea brasiliensis on oral microorganisms. Mycoses, 2008, 51(4), 301-307.
[] [PMID: 18924261]
Mavlonov, G.T.; Ubaidullaeva, K.A.; Rakhmanov, M.I.; Abdurakhmonov, I.Y.; Abdukarimov, A. Chitin-Binding Antifungal Protein from Ficus carica Latex. Chem. Nat. Compd., 2008, 44(2), 216-219.
Van Deenen, N.; Prüfer, D.; Gronover, C.S. A Latex Lectin from Euphorbia trigona Is a Potent Inhibitor of Fungal Growth. Biol. Plant., 2011, 55(2), 335-339.
Gai, Y-P.; Zhao, Y-N.; Zhao, H-N.; Yuan, C-Z.; Yuan, S-S.; Li, S.; Zhu, B-S.; Ji, X-L. The Latex Protein MLX56 from Mulberry (Morus multicaulis) Protects Plants against Insect Pests and Pathogens. Front. Plant Sci., 2017, 8, 1475.
[] [PMID: 28878804]
Hoffmann-Sommergruber, K. Plant allergens and pathogenesis-related proteins. What do they have in common? Int. Arch. Allergy Immunol., 2000, 122(3), 155-166.
[] [PMID: 10899758]
Viktorova, J.; Krasny, L.; Kamlar, M.; Novakova, M.; Mackova, M.; Macek, T. Osmotin, a pathogenesis-related protein. Curr. Protein Pept. Sci., 2012, 13(7), 672-681.
[] [PMID: 23061797]
Misra, R.C.; Sandeep, ; Kamthan, M.; Kumar, S.; Ghosh, S. A thaumatin-like protein of Ocimum basilicum confers tolerance to fungal pathogen and abiotic stress in transgenic Arabidopsis. Sci. Rep., 2016, 6, 1-14.
Moosa, A.; Farzand, A.; Sahi, S.T.; Khan, S.A. Transgenic Expression of Antifungal Pathogenesis-Related Proteins against Phytopathogenic Fungi-15 Years of Success. Isr. J. Plant Sci., 2017, 1-17.
Anu, K.; Jessymol, K.K.; Chidambareswaren, M.; Gayathri, G.S.; Manjula, S. Down-regulation of osmotin (PR5) gene by virus-induced gene silencing (VIGS) leads to susceptibility of resistant Piper colubrinum Link. to the oomycete pathogen Phytophthora capsici Leonian. Indian J. Exp. Biol., 2015, 53(6), 329-334.
[PMID: 26155671]
Su, H.Y.; Chou, H.H.; Chow, T.J.; Lee, T.M.; Chang, J.S.; Huang, W.L.; Chen, H.J. Improvement of outdoor culture efficiency of cyanobacteria by over-expression of stress tolerance genes and its implication as bio-refinery feedstock. Bioresour. Technol., 2017, 244(Pt 2), 1294-1303.
[] [PMID: 28457721]
Anil Kumar, S.; Hima Kumari, P.; Shravan Kumar, G.; Mohanalatha, C.; Kavi Kishor, P.B. Osmotin: a plant sentinel and a possible agonist of mammalian adiponectin. Front. Plant Sci., 2015, 6(163), 163.
[] [PMID: 25852715]
Abad, L.R.; D’Urzo, M.P.; Liu, D.; Narasimhan, M.L.; Reuveni, M.; Zhu, J.K.; Niu, X.; Singh, N.K.; Hasegawa, P.M.; Bressan, R.A. Antifungal Activity of Tobacco Osmotin Has Specificity and Involves Plasma Membrane Permeabilization. Plant Sci., 1996, 118(1), 11-23.
Yun, D.J.; Ibeas, J.I.; Lee, H.; Coca, M.A.; Narasimhan, M.L.; Uesono, Y.; Hasegawa, P.M.; Pardo, J.M.; Bressan, R.A. Osmotin, a plant antifungal protein, subverts signal transduction to enhance fungal cell susceptibility. Mol. Cell, 1998, 1(6), 807-817.
[] [PMID: 9660964]
Yun, D.J.; Bressan, R.A.; Hasegawa, P.M. Plant Antifungal Proteins. Plant Breed. Rev., 1997, 14, 39-88.
[PMID: 9192695]
Chowdhury, S.; Basu, A.; Kundu, S. Cloning, characterization, and bacterial over-expression of an osmotin-like protein gene from Solanum nigrum L. with antifungal activity against three necrotrophic fungi. Mol. Biotechnol., 2015, 57(4), 371-381.
[] [PMID: 25572937]
Bartnicki-Garcia, S. Cell wall chemistry, morphogenesis, and taxonomy of fungi. Annu. Rev. Microbiol., 1968, 22, 87-108.
[] [PMID: 4879523]
Shi, M.; Li, Y.; Deng, S.; Wang, D.; Chen, Y.; Yang, S.; Wu, J.; Tian, W.M. The formation and accumulation of protein-networks by physical interactions in the rapid occlusion of laticifer cells in rubber tree undergoing successive mechanical wounding. BMC Plant Biol., 2019, 19(1), 8.
[] [PMID: 30616545]
Moulin-Traffort, J.; Giordani, R.; Régli, P. Antifungal action of latex saps from Lactuca sativa L. and Asclepias curassavica L. Mycoses, 1990, 33(7-8), 383-392.
[] [PMID: 2090937]
Henrissat, B. Glycosidase families. Biochem. Soc. Trans., 1998, 26(2), 153-156.
[] [PMID: 9649738]
Giordani, R.; Siepaio, M.; Moulin-Traffort, J.; Régli, P. Antifungal action of Carica papaya latex: isolation of fungal cell wall hydrolysing enzymes. Mycoses, 1991, 34(11-12), 469-477.
[] [PMID: 1824416]
Sritanyarat, W.; Pearce, G.; Siems, W.F.; Ryan, C.A.; Wititsuwannakul, R.; Wititsuwannakul, D. Isolation and characterization of isoinhibitors of the potato protease inhibitor I family from the latex of the rubber trees, Hevea brasiliensis. Phytochemistry, 2006, 67(15), 1644-1650.
[] [PMID: 16438995]
Citores, L.; Iglesias, R.; Gay, C.; Ferreras, J.M. Antifungal activity of the ribosome-inactivating protein BE27 from sugar beet (Beta vulgaris L.) against the green mould Penicillium digitatum. Mol. Plant Pathol., 2016, 17(2), 261-271.
[] [PMID: 25976013]
Ready, M.P.; Brown, D.T.; Robertus, J.D. Extracellular localization of pokeweed antiviral protein. Proc. Natl. Acad. Sci. USA, 1986, 83(14), 5053-5056.
[] [PMID: 3523481]
Bolognesi, A.; Bortolotti, M.; Maiello, S.; Battelli, M.G.; Polito, L. Ribosome-Inactivating Proteins from Plants: A Historical Overview. Molecules, 2016, 21(12), E1627
[] [PMID: 27898041]
Terwisscha van Scheltinga, A.C.; Hennig, M.; Dijkstra, B.W. The 1.8 A resolution structure of hevamine, a plant chitinase/lysozyme, and analysis of the conserved sequence and structure motifs of glycosyl hydrolase family 18. J. Mol. Biol., 1996, 262(2), 243-257.
[] [PMID: 8831791]
Martínez-Caballero, S.; Cano-Sánchez, P.; Mares-Mejía, I.; Díaz-Sánchez, A.G.; Macías-Rubalcava, M.L.; Hermoso, J.A.; Rodríguez-Romero, A. Comparative study of two GH19 chitinase-like proteins from Hevea brasiliensis, one exhibiting a novel carbohydrate-binding domain. FEBS J., 2014, 281(19), 4535-4554.
[] [PMID: 25104038]
Moreno, F. B. M. B.; Oliveira, R. S. B.; Moreira, R. A.; Lobo, M.D. P.; Freitas, C. D. T.; Ramos, M. V.; Grangeiro, T. B. Monteiro- Moreira, A. C. O. Crystal Structure of an Antifungal Laticifer Protein, 2014.
Kamphuis, I.G.; Kalk, K.H.; Swarte, M.B.; Drenth, J. Structure of papain refined at 1.65 A resolution. J. Mol. Biol., 1984, 179(2), 233-256.
[] [PMID: 6502713]
Azarkan, M.; Martinez-Rodriguez, S.; Buts, L.; Baeyens-Volant, D.; Garcia-Pino, A. The plasticity of the β-trefoil fold constitutes an evolutionary platform for protease inhibition. J. Biol. Chem., 2011, 286(51), 43726-43734.
[] [PMID: 22027836]

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Year: 2020
Page: [497 - 506]
Pages: 10
DOI: 10.2174/1389203720666191119101756
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