PATHOGENESIS-RELATED PROTEINS IN PLANTS: MOLECULAR FEATURES, FUNCTIONAL DIVERSITY, AND BIOTECHNOLOGICAL APPLICATIONS
DOI:
https://doi.org/10.64013/jpbab.v2026i1.52Keywords:
chitinases, glucanases, defensins, thionins; fungi, bacteria, oomycetes, viruses, Pathogenesis-related (PR) proteinsAbstract
Pathogenesis-related (PR) proteins are critical components of the plant immune system, rapidly accumulating in response to pathogen attack and various stresses. Since their first identification in tobacco infected with Tobacco Mosaic Virus (TMV), these inducible proteins have been classified into multiple families based on sequence and functional characteristics. PR proteins exhibit a range of biochemical activities – including cell-wall degrading enzyme activities (e.g., chitinases, glucanases), antimicrobial peptide functions (e.g., defensins, thionins), and protease inhibition – that contribute to direct pathogen suppression and modulation of defense signaling. Advances in molecular cloning have enabled transgenic expression of PR genes in susceptible crops, often leading to enhanced resistance against fungi, bacteria, oomycetes, and viruses. Beyond plant immunity, some PR proteins display multifunctional properties relevant to stress tolerance and pharmacology. This review summarizes current understanding of PR protein classification, molecular features, induction by biotic/abiotic cues, and their application in crop protection, while highlighting opportunities and challenges in harnessing PR proteins for biotechnology.
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Ahl, P., Cornu, A., and Gianinazzi, S. (1982). Soluble proteins as genetic markers in studies of resistance and phylogeny in Nicotiana. Phytopathology 72, 80-85. DOI: https://doi.org/10.1094/Phyto-72-80
Ahl, P., and Gianinazzi, S. (1982). b-Protein as a constitutive component in highly (TMV) resistant interspecific hybrids of Nicotiana glutinosa× Nicotiana debneyi. Plant Science Letters 26, 173-181. DOI: https://doi.org/10.1016/0304-4211(82)90089-X
Alazem, M., and Lin, N. S. (2015). Roles of plant hormones in the regulation of host–virus interactions. Molecular plant pathology 16, 529-540. DOI: https://doi.org/10.1111/mpp.12204
Alblas, S., and De, R. (1986). Induction by salicylic acid of pathogenesis-related proteins and resistance to alfalfa mosaic virus infection in various plant species.
Alexander, D., Goodman, R. M., Gut-Rella, M., Glascock, C., Weymann, K., Friedrich, L., Maddox, D., Ahl-Goy, P., Luntz, T., and Ward, E. (1993). Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. Proceedings of the National Academy of Sciences 90, 7327-7331. DOI: https://doi.org/10.1073/pnas.90.15.7327
Alkooranee, J. T., Aledan, T. R., Ali, A. K., Lu, G., Zhang, X., Wu, J., Fu, C., and Li, M. (2017). Detecting the hormonal pathways in oilseed rape behind induced systemic resistance by Trichoderma harzianum TH12 to Sclerotinia sclerotiorum. PloS one 12, e0168850. DOI: https://doi.org/10.1371/journal.pone.0168850
Antoniw, J., Ritter, C., Pierpoint, W., and Van Loon, L. (1980). Comparison of three pathogenesis-related proteins from plants of two cultivars of tobacco infected with TMV. Journal of General Virology 47, 79-87. DOI: https://doi.org/10.1099/0022-1317-47-1-79
Asao, H., Nishizawa, Y., Arai, S., SATO, T., HIRAI, M., YOSHIDA, K., SHINMYO, A., and HIBI, T. (1997). Enhanced resistance against a fungal pathogen Sphaerotheca humuli in transgenic strawberry expressing a rice chitinase gene. Plant Biotechnology 14, 145-149. DOI: https://doi.org/10.5511/plantbiotechnology.14.145
Asselin, A., Grenier, J., and Côté, F. (1985). Light-influenced extracellular accumulation of b (pathogenesis-related) proteins in Nicotiana green tissue induced by various chemicals or prolonged floating on water. Canadian journal of botany 63, 1276-1283. DOI: https://doi.org/10.1139/b85-177
Athar, M., Back, J. H., Tang, X., Kim, K. H., Kopelovich, L., Bickers, D. R., and Kim, A. L. (2007). Resveratrol: a review of preclinical studies for human cancer prevention. Toxicology and applied pharmacology 224, 274-283. DOI: https://doi.org/10.1016/j.taap.2006.12.025
Bai, X., Long, J., He, X., Li, S., and Xu, H. (2014). Molecular cloning and characterization of pathogenesis-related protein family 10 gene from spinach (SoPR10). Bioscience, biotechnology, and biochemistry 78, 780-786. DOI: https://doi.org/10.1080/09168451.2014.910094
Benhamou, N., Grenier, J., and Asselin, A. (1991). Immunogold localization of pathogenesis-related protein P14 in tomato root cells infected by Fusarium oxysporum f. sp. radicis-lycopersici. Physiological and Molecular Plant Pathology 38, 237-253. DOI: https://doi.org/10.1016/S0885-5765(05)80116-X
Berrocal-Lobo, M., Molina, A., Rodríguez-Palenzuela, P., García-Olmedo, F., and Rivas, L. (2009). Leishmania donovani: thionins, plant antimicrobial peptides with leishmanicidal activity. Experimental parasitology 122, 247-249. DOI: https://doi.org/10.1016/j.exppara.2009.03.019
Bryngelsson, T., and Green, B. (1989). Characterization of a pathogenesis-related, thaumatin-like protein isolated from barley challenged with an incompatible race of mildew. Physiological and molecular plant pathology 35, 45-52. DOI: https://doi.org/10.1016/0885-5765(89)90006-4
Buchel, A. S., and Linthorst, H. J. (1999). 2 PR-Proteins Induced Upon Pathogen Infection. PATHOGENESIS-RELATED PROTEINS IN PLANTS. DOI: https://doi.org/10.1201/9781420049299.ch2
Campos, M. A., Rosa, D. D., Teixeira, J. É. C., Targon, M. L. P., Souza, A. A., Paiva, L. V., Stach-Machado, D. R., and Machado, M. A. (2007). PR gene families of citrus: their organ specific-biotic and abiotic inducible expression profiles based on ESTs approach. Genetics and Molecular Biology 30, 917-930. DOI: https://doi.org/10.1590/S1415-47572007000500020
Caporale, C., Di Berardino, I., Leonardi, L., Bertini, L., Cascone, A., Buonocore, V., and Caruso, C. (2004). Wheat pathogenesis‐related proteins of class 4 have ribonuclease activity. Febs Letters 575, 71-76. DOI: https://doi.org/10.1016/j.febslet.2004.07.091
Chen, Z.-Y., Brown, R., Rajasekaran, K., Damann, K., and Cleveland, T. (2006). Identification of a maize kernel pathogenesis-related protein and evidence for its involvement in resistance to Aspergillus flavus infection and aflatoxin production. Phytopathology 96, 87-95. DOI: https://doi.org/10.1094/PHYTO-96-0087
Chisholm, S. T., Coaker, G., Day, B., and Staskawicz, B. J. (2006). Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803-814. DOI: https://doi.org/10.1016/j.cell.2006.02.008
Condit, C. M., and Meagher, R. B. (1986). A gene encoding a novel glycine-rich structural protein of petunia. Nature 323, 178-181. DOI: https://doi.org/10.1038/323178a0
Conejero, V., Picazo, I., and Segado, P. (1979). Citrus exocortis viroid (CEV): protein alterations in different hosts following viroid infection. Virology 97, 454-456. DOI: https://doi.org/10.1016/0042-6822(79)90355-6
Datta, K., Tu, J., Oliva, N., Ona, I., Velazhahan, R., Mew, T. W., Muthukrishnan, S., and Datta, S. K. (2001). Enhanced resistance to sheath blight by constitutive expression of infection-related rice chitinase in transgenic elite indica rice cultivars. Plant Science 160, 405-414. DOI: https://doi.org/10.1016/S0168-9452(00)00413-1
Datta, K., Velazhahan, R., Oliva, N., Ona, I., Mew, T., Khush, G., Muthukrishnan, S., and Datta, S. (1999). Over-expression of the cloned rice thaumatin-like protein (PR-5) gene in transgenic rice plants enhances environmental friendly resistance to Rhizoctonia solani causing sheath blight disease. TAG Theoretical and Applied Genetics 98, 1138-1145. DOI: https://doi.org/10.1007/s001220051178
Datta, S. K., and Muthukrishnan, S. (1999). "Pathogenesis-related proteins in plants," CRC press. DOI: https://doi.org/10.1201/9781420049299
DeYoung, B. J., and Innes, R. W. (2006). Plant NBS-LRR proteins in pathogen sensing and host defense. Nature immunology 7, 1243-1249. DOI: https://doi.org/10.1038/ni1410
Dixelius, C. (1994). Presence of the pathogenesis-related proteins 2, Q and S in stressed Brassica napus and B. nigra plantlets. Physiological and Molecular Plant Pathology 44, 1-8. DOI: https://doi.org/10.1016/S0885-5765(05)80090-6
Du, X., Wang, S., Gao, F., Zhang, L., Zhao, J.-H., Guo, H.-S., and Hua, C. (2017). Expression of pathogenesis-related genes in cotton roots in response to Verticillium dahliae PAMP molecules. Science China Life Sciences 60, 852-860. DOI: https://doi.org/10.1007/s11427-017-9071-9
Eckey-Kaltenbach, H., Kiefer, E., Grosskopf, E., Ernst, D., and Sandermann, H. (1997). Differential transcript induction of parsley pathogenesis-related proteins and of a small heat shock protein by ozone and heat shock. Plant molecular biology 33, 343-350. DOI: https://doi.org/10.1023/A:1005786317975
Edreva, A. (2005). Pathogenesis-related proteins: research progress in the last 15 years. Gen Appl Plant Physiol 31, 105-24.
EDREVA, A. M. (1990). Induction of ‘pathogenesis-related’proteins in tobacco leaves by physiological (non-pathogenic) disorders. Journal of experimental botany 41, 701-703. DOI: https://doi.org/10.1093/jxb/41.6.701
Enoki, S., and Suzuki, S. (2016). Pathogenesis-Related Proteins in Grape. In "Grape and Wine Biotechnology". InTech. DOI: https://doi.org/10.5772/64873
Fagoaga, C., Rodrigo, I., Conejero, V., Hinarejos, C., Tuset, J. J., Arnau, J., Pina, J. A., Navarro, L., and Peña, L. (2001). Increased tolerance to Phytophthora citrophthora in transgenic orange plants constitutively expressing a tomato pathogenesis related protein PR-5. Molecular Breeding 7, 175-185. DOI: https://doi.org/10.1023/A:1011358005054
Fanta, N., Ortega, X., and Perez, L. M. (2003). The development of Alternaria alternata is prevented by chitinases and ß-1, 3-glucanases from Citrus limon seedlings. Biological research 36, 411-420. DOI: https://doi.org/10.4067/S0716-97602003000300012
Fernández, C., Szyperski, T., Bruyere, T., Ramage, P., Mösinger, E., and Wüthrich, K. (1997). NMR solution structure of the pathogenesis-related protein P14a. Journal of molecular biology 266, 576-593. DOI: https://doi.org/10.1006/jmbi.1996.0772
Freitas, L. B. d., Koehler-Santos, P., and Salzano, F. M. (2003). Pathogenesis-related proteins in Brazilian wheat genotypes: protein induction and partial gene sequencing. Ciência Rural 33, 497-500. DOI: https://doi.org/10.1590/S0103-84782003000300016
Fujibe, T., Watanabe, K., Nakajima, N., Ohashi, Y., Mitsuhara, I., Yamamoto, K. T., and Takeuchi, Y. (2000). Accumulation of pathogenesis-related proteins in tobacco leaves irradiated with UV-B. Journal of Plant Research 113, 387-394. DOI: https://doi.org/10.1007/PL00013946
Fulda, S., and Debatin, K.-M. (2004). Sensitization for tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by the chemopreventive agent resveratrol. Cancer research 64, 337-346. DOI: https://doi.org/10.1158/0008-5472.CAN-03-1656
Gianinazzi, S. (1982). Antiviral agents and inducers of virus resistance: analogies with interferon. In "Active defense mechanisms in plants", pp. 275-298. Springer. DOI: https://doi.org/10.1007/978-1-4615-8309-7_15
Gianinazzi, S., Martin, C., and Vallee, J. (1970). Hypersensibilite aux virus, temperature et proteines solubles chez le Nicotiana xanthi n. c: apparition de nouvelles macromolecules lors de la repression de la synthese virale. Acad Sci Paris CR Ser D.
Gianinazzi, S., Pratt, H. M., Shewry, P., and Miflin, B. (1977). Partial purification and preliminary characterization of soluble leaf proteins specific to virus infected tobacco plants. Journal of General Virology 34, 345-351. DOI: https://doi.org/10.1099/0022-1317-34-2-345
González-Lamothe, R., Mitchell, G., Gattuso, M., Diarra, M. S., Malouin, F., and Bouarab, K. (2009). Plant antimicrobial agents and their effects on plant and human pathogens. International Journal of Molecular Sciences 10, 3400-3419. DOI: https://doi.org/10.3390/ijms10083400
Grenier, J., Potvin, C., and Asselin, A. (1993). Barley pathogenesis-related proteins with fungal cell wall lytic activity inhibit the growth of yeasts. Plant physiology 103, 1277-1283. DOI: https://doi.org/10.1104/pp.103.4.1277
GRÜNER, R., and PFITZNER, U. M. (1994). The upstream region of the gene for the pathogenesis‐related protein 1 a from tobacco responds to environmental as well as to developmental signals in transgenic plants. The FEBS Journal 220, 247-255. DOI: https://doi.org/10.1111/j.1432-1033.1994.tb18620.x
Henriquez, A. C., and Sänger, H. (1982). Gelelectrophoretic analysis of phenol-extractable leaf proteins from different viroid/host combinations. Archives of virology 74, 167-180. DOI: https://doi.org/10.1007/BF01314710
Henrissat, B., and Bairoch, A. (1993). New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochemical journal 293, 781-788. DOI: https://doi.org/10.1042/bj2930781
Hill, A. J., Peikin, S. R., Ryan, C. A., and Blundell, J. E. (1990). Oral administration of proteinase inhibitor II from potatoes reduces energy intake in man. Physiology & behavior 48, 241-246. DOI: https://doi.org/10.1016/0031-9384(90)90307-P
Jang, M., Cai, L., Udeani, G. O., Slowing, K. V., Thomas, C. F., Beecher, C. W., Fong, H. H., Farnsworth, N. R., Kinghorn, A. D., and Mehta, R. G. (1997). Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275, 218-220. DOI: https://doi.org/10.1126/science.275.5297.218
Jeandet, P., Hébrard, C., Deville, M.-A., Cordelier, S., Dorey, S., Aziz, A., and Crouzet, J. (2014). Deciphering the role of phytoalexins in plant-microorganism interactions and human health. Molecules 19, 18033-18056. DOI: https://doi.org/10.3390/molecules191118033
Jeun, Y.-C. (2000). Immunolocalization of PR-protein P14 in leaves of tomato plants exhibiting systemic acquired resistance against Phytophthora infestans induced by pretreatment with 3-aminobutryic acid and preinoculation with Tobacco necrosis virus/Immunolokalisierung des PR-Proteins P14 in Blättern von Tomatenpflanzen mit systemisch erworbener Resistenz gegenüber Phytophthora infestans induziert durch Vorbehandlung mit 3-Amimobuttersäure und Vorinokulation mit Tabaknekrosevirus. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz/Journal of Plant Diseases and Protection, 352-367.
Jeun, Y., and Buchenauer, H. (2001). Infection Structures and Localization of the Pathogenesis-related Protein AP 24 in Leaves of Tomato Plants Exhibiting Systemic Acquired Resistance against Phytophthora infestans after Pre-treatment with 3-Aminobutyric acid or Tobacco Necrosis Virus. Journal of Phytopathology 149, 141-154. DOI: https://doi.org/10.1046/j.1439-0434.2001.00594.x
Jung, J.-l., Fritig, B., and Hahne, G. (1993). Sunflower (Helianthus annuus L.) Pathogenesis-related proteins (induction by aspirin (acetylsalicylic Acid) and characterization). Plant physiology 101, 873-880. DOI: https://doi.org/10.1104/pp.101.3.873
Kärenlampi, S. O., Airaksinen, K., Miettinen, A. T., Kokko, H. I., Holopainen, J. K., Kärenlampi, L. V., and Karjalainen, R. O. (1994). Pathogenesis‐related proteins in ozone‐exposed Norway spruce [Picea abies (Karst) L.]. New Phytologist 126, 81-89. DOI: https://doi.org/10.1111/j.1469-8137.1994.tb07532.x
Kello, M., Drutovic, D., Chripkova, M., Pilatova, M., Budovska, M., Kulikova, L., Urdzik, P., and Mojzis, J. (2014). ROS-dependent antiproliferative effect of brassinin derivative homobrassinin in human colorectal cancer Caco2 cells. Molecules 19, 10877-10897. DOI: https://doi.org/10.3390/molecules190810877
Khanal, P., Karmacharya, A., Sharma, S., Nepal, A. K., and Shrestha, K. (2014). Biotechnological production of inducible defense-related proteins in edible radish (Raphanus sativus) found in Nepal. Journal of clinical and diagnostic research: JCDR 8, 112. DOI: https://doi.org/10.7860/JCDR/2014/6788.3956
King, G. J., Turner, V. A., Hussey, C. E., Wurtele, E. S., and Lee, S. M. (1988). Isolation and characterization of a tomato cDNA clone which codes for a salt-induced protein. Plant molecular biology 10, 401-412. DOI: https://doi.org/10.1007/BF00014946
Kirubakaran, S. I., and Sakthivel, N. (2007). Cloning and overexpression of antifungal barley chitinase gene in Escherichia coli. Protein expression and purification 52, 159-166. DOI: https://doi.org/10.1016/j.pep.2006.08.012
Ko, K., Norelli, J. L., Brown, S. K., and Aldwinckle, H. S. (1999). Anti-attacin polyclonal antibody from an in vitro derived antigen used for immunoblot to quantify attacin expressed in transgenic apple. Biotechnology techniques 13, 849-857. DOI: https://doi.org/10.1023/A:1008924207786
Ko, K., Norelli, J. L., Reynoird, J.-P., Boresjza-Wysocka, E., Brown, S. K., and Aldwinckle, H. S. (2000). Effect of untranslated leader sequence of AMV RNA 4 and signal peptide of pathogenesis-related protein 1b on attacin gene expression, and resistance to fire blight in transgenic apple. Biotechnology Letters 22, 373-381. DOI: https://doi.org/10.1023/A:1005672601625
Koiwa, H., Bressan, R. A., and Hasegawa, P. M. (1997). Regulation of protease inhibitors and plant defense. Trends in Plant Science 2, 379-384. DOI: https://doi.org/10.1016/S1360-1385(97)90052-2
Kombrink, E., and Somssich, I. (1997). Pathogenesis-related proteins and plant defense. In "Plant relationships", pp. 107-128. Springer. DOI: https://doi.org/10.1007/978-3-662-10370-8_7
Lin, P., Xia, L., Wong, J. H., Ng, T., Ye, X., Wang, S., and Xiangzhu, S. (2007). Lipid transfer proteins from Brassica campestris and mung bean surpass mung bean chitinase in exploitability. Journal of Peptide Science 13, 642-648. DOI: https://doi.org/10.1002/psc.893
Linthorst, H., Meuwissen, R., Kauffmann, S., and Bol, J. F. (1989). Constitutive expression of pathogenesis-related proteins PR-1, GRP, and PR-S in tobacco has no effect on virus infection. The Plant Cell 1, 285-291. DOI: https://doi.org/10.1105/tpc.1.3.285
Liu, D., Raghothama, K. G., Hasegawa, P. M., and Bressan, R. A. (1994). Osmotin overexpression in potato delays development of disease symptoms. Proceedings of the National Academy of Sciences 91, 1888-1892. DOI: https://doi.org/10.1073/pnas.91.5.1888
Loeza-Ángeles, H., Sagrero-Cisneros, E., Lara-Zárate, L., Villagómez-Gómez, E., López-Meza, J. E., and Ochoa-Zarzosa, A. (2008). Thionin Thi2. 1 from Arabidopsis thaliana expressed in endothelial cells shows antibacterial, antifungal and cytotoxic activity. Biotechnology Letters 30, 1713. DOI: https://doi.org/10.1007/s10529-008-9756-8
Lozano-Mena, G., Sánchez-González, M., Juan, M. E., and Planas, J. M. (2014). Maslinic acid, a natural phytoalexin-type triterpene from olives—a promising nutraceutical? Molecules 19, 11538-11559. DOI: https://doi.org/10.3390/molecules190811538
Luo, M., Wang, Z., Li, H., Xia, K.-F., Cai, Y., and Xu, Z.-F. (2009). Overexpression of a weed (Solanum americanum) proteinase inhibitor in transgenic tobacco results in increased glandular trichome density and enhanced resistance to Helicoverpa armigera and Spodoptera litura. International journal of molecular sciences 10, 1896-1910. DOI: https://doi.org/10.3390/ijms10041896
Mao, Y.-B., Xue, X.-Y., Tao, X.-Y., Yang, C.-Q., Wang, L.-J., and Chen, X.-Y. (2013). Cysteine protease enhances plant-mediated bollworm RNA interference. Plant molecular biology 83, 119-129. DOI: https://doi.org/10.1007/s11103-013-0030-7
Miele, M., Costantini, S., and Colonna, G. (2011). Structural and functional similarities between osmotin from Nicotiana tabacum seeds and human adiponectin. PLoS One 6, e16690. DOI: https://doi.org/10.1371/journal.pone.0016690
MINIC, Z., BROWN, S., De KOUCHKOVSKY, Y., SCHULTZE, M., and STAEHELIN, C. (1998). Purification and characterization of a novel chitinase–lysozyme, of another chitinase, both hydrolysing Rhizobium meliloti Nod factors, and of a pathogenesis-related protein from Medicago sativa roots. Biochemical journal 332, 329-335. DOI: https://doi.org/10.1042/bj3320329
Narusaka, M., Kubo, Y., Hatakeyama, K., Imamura, J., Ezura, H., Nanasato, Y., Tabei, Y., Takano, Y., Shirasu, K., and Narusaka, Y. (2013). Interfamily transfer of dual NB-LRR genes confers resistance to multiple pathogens. PLoS One 8, e55954. DOI: https://doi.org/10.1371/journal.pone.0055954
Nasser, W., de Tapia, M., Kauffmann, S., Montasser-Kouhsari, S., and Burkard, G. (1988). Identification and characterization of maize pathogenesis-related proteins. Four maize PR proteins are chitinases. Plant Molecular Biology 11, 529-538. DOI: https://doi.org/10.1007/BF00039033
Ooi, L. S., Tian, L., Su, M., Ho, W.-S., Sun, S. S., Chung, H.-Y., Wong, H. N., and Ooi, V. E. (2008). Isolation, characterization, molecular cloning and modeling of a new lipid transfer protein with antiviral and antiproliferative activities from Narcissus tazetta. Peptides 29, 2101-2109. DOI: https://doi.org/10.1016/j.peptides.2008.08.020
Ou, S. H. (1985). "Rice diseases," IRRI.
Pääkkönen, E., Seppänen, S., Holopainen, T., Kokko, H., Kärenlampi, S., Kärenlampi, L., and Kangasjärvi, J. (1998). Induction of genes for the stress proteins PR-10 and PAL in relation to growth, visible injuries and stomatal conductance in birch (Betula pendula) clones exposed to ozone and/or drought. The New Phytologist 138, 295-305. DOI: https://doi.org/10.1046/j.1469-8137.1998.00898.x
Pečenková, T., Pleskot, R., and Žárský, V. (2017). Subcellular localization of Arabidopsis pathogenesis-related 1 (PR1) protein. International Journal of Molecular Sciences 18, 825. DOI: https://doi.org/10.3390/ijms18040825
Pennazio, S. (1981). Changes in the soluble protein constitution of Gomphrena globosa leaves showing spontaneous local lesions. Rivista di Patologia Vegetale, 127-135.
Pierpoint, W., Tatham, A., and Pappin, D. (1987). Identification of the virus-induced protein of tobacco leaves that resembles the sweet-protein thaumatin. Physiological and molecular plant pathology 31, 291-298. DOI: https://doi.org/10.1016/0885-5765(87)90072-5
Rathore, A. S., and Gupta, R. D. (2015). Chitinases from bacteria to human: properties, applications, and future perspectives. Enzyme research 2015. DOI: https://doi.org/10.1155/2015/791907
Redolfi, P., and Cantisani, A. (1984). Preliminary characterization of new soluble proteins in Phaseolus vulgaris cv. Saxa reacting hypersensitively to viral infection. Physiological plant pathology 25, 9-19. DOI: https://doi.org/10.1016/0048-4059(84)90014-6
Reiss, E., and Bryngelsson, T. (1996). Pathogenesis-related proteins in barley leaves, induced by infection withDrechslera teres (Sacc.) Shoem. and by treatment with other biotic agents. Physiological and molecular plant pathology 49, 331-341. DOI: https://doi.org/10.1006/pmpp.1996.0058
Rodrigo, I., Vera, P., Frank, R., and Conejero, V. (1991). Identification of the viroid-induced tomato pathogenesis-related (PR) protein P23 as the thaumatin-like tomato protein NP24 associated with osmotic stress. Plant molecular biology 16, 931-934. DOI: https://doi.org/10.1007/BF00015088
Ruseler‐van Embden, J. G. H., Van Lieshout, L., Smits, S., Van Kessel, I., and Laman, J. (2004). Potato tuber proteins efficiently inhibit human faecal proteolytic activity: implications for treatment of peri‐anal dermatitis. European journal of clinical investigation 34, 303-311. DOI: https://doi.org/10.1111/j.1365-2362.2004.01330.x
Ryals, J., Uknes, S., and Ward, E. (1994). Systemic acquired resistance. Plant Physiology 104, 1109. DOI: https://doi.org/10.1104/pp.104.4.1109
Sahai, A., and Manocha, M. (1993). Chitinases of fungi and plants: their involvement in morphogenesis and host‐parasite interaction. FEMS Microbiology Reviews 11, 317-338. DOI: https://doi.org/10.1111/j.1574-6976.1993.tb00004.x
Sarowar, S., Kim, Y. J., Kim, E. N., Kim, K. D., Hwang, B. K., Islam, R., and Shin, J. S. (2005). Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant cell reports 24, 216-224. DOI: https://doi.org/10.1007/s00299-005-0928-x
Schestibratov, K., and Dolgov, S. (2005). Transgenic strawberry plants expressing a thaumatin II gene demonstrate enhanced resistance to Botrytis cinerea. Scientia Horticulturae 106, 177-189. DOI: https://doi.org/10.1016/j.scienta.2005.03.016
Singh, N. K., Bracker, C. A., Hasegawa, P. M., Handa, A. K., Buckel, S., Hermodson, M. A., Pfankoch, E., Regnier, F. E., and Bressan, R. A. (1987). Characterization of osmotin A thaumatin-like protein associated with osmotic adaptation in plant cells. Plant physiology 85, 529-536. DOI: https://doi.org/10.1104/pp.85.2.529
Singh, N. K., Kumar, K. R. R., Kumar, D., Shukla, P., and Kirti, P. (2013). Characterization of a pathogen induced thaumatin-like protein gene AdTLP from Arachis diogoi, a wild peanut. PloS one 8, e83963. DOI: https://doi.org/10.1371/journal.pone.0083963
Singh, R., Tiwari, J., Sharma, V., Singh, B., Rawat, S., and Singh, R. (2014). Role of Pathogen related protein families in defence mechanism with potential role in applied biotechnology. International Journal of Advanced Research 2, 210-226.
Smith, B., Randle, D., Mezencev, R., Thomas, L., Hinton, C., and Odero-Marah, V. (2014). Camalexin-induced apoptosis in prostate cancer cells involves alterations of expression and activity of lysosomal protease cathepsin D. Molecules 19, 3988-4005. DOI: https://doi.org/10.3390/molecules19043988
Su, Y.-c., Xu, L.-p., Xue, B.-t., Wu, Q.-b., Guo, J.-l., Wu, L.-g., and Que, Y.-x. (2013). Molecular cloning and characterization of two pathogenesis-related β-1, 3-glucanase genes ScGluA1 and ScGluD1 from sugarcane infected by Sporisorium scitamineum. Plant cell reports 32, 1503-1519. DOI: https://doi.org/10.1007/s00299-013-1463-9
Tabei, Y., Kitade, S., Nishizawa, Y., Kikuchi, N., Kayano, T., Hibi, T., and Akutsu, K. (1998). Transgenic cucumber plants harboring a rice chitinase gene exhibit enhanced resistance to gray mold (Botrytis cinerea). Plant Cell Reports 17, 159-164. DOI: https://doi.org/10.1007/s002990050371
Takatsu, Y., Nishizawa, Y., Hibi, T., and Akutsu, K. (1999). Transgenic chrysanthemum (Dendranthema grandiflorum (Ramat.) Kitamura) expressing a rice chitinase gene shows enhanced resistance to gray mold (Botrytis cinerea). Scientia Horticulturae 82, 113-123. DOI: https://doi.org/10.1016/S0304-4238(99)00034-5
Tamás, L., Huttová, J., and Žigová, Z. (1997). Accumulation of stress-proteins in intercellular spaces of barley leaves induced by biotic and abiotic factors. Biologia plantarum 39, 387-394. DOI: https://doi.org/10.1023/A:1001028226434
Tas, P., and Peters, D. (1977). The occurrence of a soluble protein (E1) in cucumber cotyledons infected with plant viruses. Netherlands Journal of Plant Pathology 83, 5-12. DOI: https://doi.org/10.1007/BF01976507
Taveira, G. B., Mathias, L. S., Motta, O. V., Machado, O. L., Rodrigues, R., Carvalho, A. O., Teixeira‐Ferreira, A., Perales, J., Vasconcelos, I. M., and Gomes, V. M. (2014). Thionin‐like peptides from Capsicum annuum fruits with high activity against human pathogenic bacteria and yeasts. Peptide Science 102, 30-39. DOI: https://doi.org/10.1002/bip.22351
Van Huijsduijnen, R. H., Van Loon, L., and Bol, J. (1986). cDNA cloning of six mRNAs induced by TMV infection of tobacco and a characterization of their translation products. The EMBO journal 5, 2057. DOI: https://doi.org/10.1002/j.1460-2075.1986.tb04466.x
Van Loon, L., Gerritsen, Y., and Ritter, C. (1987). Identification, purification, and characterization of pathogenesis-related proteins from virus-infected Samsun NN tobacco leaves. Plant Molecular Biology 9, 593-609. DOI: https://doi.org/10.1007/BF00020536
Van Loon, L., and Van Kammen, A. (1970). Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var.‘Samsun’and ‘Samsun NN’: II. Changes in protein constitution after infection with tobacco mosaic virus. Virology 40, 199-211. DOI: https://doi.org/10.1016/0042-6822(70)90395-8
Van Loon, L., and Van Strien, E. (1999). The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiological and molecular plant pathology 55, 85-97. DOI: https://doi.org/10.1006/pmpp.1999.0213
van Loon, L. C. (1985). Pathogenesis-related proteins. Plant Molecular Biology 4, 111-116. DOI: https://doi.org/10.1007/BF02418757
Varner, J., and Cassab, G. (1986). Molecular biology: A new protein in petunia. Nature 323, 110-110. DOI: https://doi.org/10.1038/323110a0
Vega, K., and Kalkum, M. (2011). Chitin, chitinase responses, and invasive fungal infections. International journal of microbiology 2012. DOI: https://doi.org/10.1155/2012/920459
Vierheilig, H., Alt, M., Lange, J., Gut-Rella, M., Wiemken, A., and Boller, T. (1995). Colonization of transgenic tobacco constitutively expressing pathogenesis-related proteins by the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Applied and Environmental Microbiology 61, 3031-3034. DOI: https://doi.org/10.1128/aem.61.8.3031-3034.1995
Viktorova, J., Krasny, L., Kamlar, M., Novakova, M., Mackova, M., and Macek, T. (2012). Osmotin, a pathogenesis-related protein. Current Protein and Peptide Science 13, 672-681. DOI: https://doi.org/10.2174/138920312804142129
Wagih, E., and Coutts, R. (1982). Comparison of Virus‐Elicited and Other Stresses on the Soluble Protein Fraction of Cucumber Cotyledons. Journal of Phytopathology 104, 364-374. DOI: https://doi.org/10.1111/j.1439-0434.1982.tb00020.x
Wagih, E., and Coutts, R. H. (1981). Similarities in the soluble protein profiles of leaf tissue following either a hypersensitive reaction to virus infection or plasmolysis. Plant Science Letters 21, 61-69. DOI: https://doi.org/10.1016/0304-4211(81)90069-9
Walsh, T., Viviani, M.-A., Arathoon, E., Chiou, C., Ghannoum, M., Groll, A., and Odds, F. (2000). New targets and delivery systems for antifungal therapy. Medical Mycology 38, 335-347. DOI: https://doi.org/10.1080/714030879
Ward, E. R., Uknes, S. J., Williams, S. C., Dincher, S. S., Wiederhold, D. L., Alexander, D. C., Ahl-Goy, P., Métraux, J.-P., and Ryals, J. A. (1991). Coordinate gene activity in response to agents that induce systemic acquired resistance. The Plant Cell 3, 1085-1094. DOI: https://doi.org/10.1105/tpc.3.10.1085
Webb, K. M., Broccardo, C. J., Prenni, J. E., and Wintermantel, W. M. (2014). Proteomic profiling of sugar beet (Beta vulgaris) leaves during rhizomania compatible interactions. Proteomes 2, 208-223. DOI: https://doi.org/10.3390/proteomes2020208
Wojtasik, W., Kulma, A., Dymińska, L., Hanuza, J., Żebrowski, J., and Szopa, J. (2013). Fibres from flax overproducing β-1, 3-glucanase show increased accumulation of pectin and phenolics and thus higher antioxidant capacity. BMC biotechnology 13, 10. DOI: https://doi.org/10.1186/1472-6750-13-10
Xu, P., Jiang, L., Wu, J., Li, W., Fan, S., and Zhang, S. (2014a). Isolation and characterization of a pathogenesis-related protein 10 gene (GmPR10) with induced expression in soybean (Glycine max) during infection with Phytophthora sojae. Molecular biology reports 41, 4899-4909. DOI: https://doi.org/10.1007/s11033-014-3356-6
Xu, T.-F., Zhao, X.-C., Jiao, Y.-T., Wei, J.-Y., Wang, L., and Xu, Y. (2014b). A pathogenesis related protein, VpPR-10.1, from Vitis pseudoreticulata: an insight of its mode of antifungal activity. PloS one 9, e95102. DOI: https://doi.org/10.1371/journal.pone.0095102
Yamamoto, T., Iketani, H., Ieki, H., Nishizawa, Y., Notsuka, K., Hibi, T., Hayashi, T., and Matsuta, N. (2000). Transgenic grapevine plants expressing a rice chitinase with enhanced resistance to fungal pathogens. Plant Cell Reports 19, 639-646. DOI: https://doi.org/10.1007/s002999900174
Yang, L., Browning, J. D., and Awika, J. M. (2009). Sorghum 3-deoxyanthocyanins possess strong phase II enzyme inducer activity and cancer cell growth inhibition properties. Journal of agricultural and food chemistry 57, 1797-1804. DOI: https://doi.org/10.1021/jf8035066
Yedidia, I., Benhamou, N., Kapulnik, Y., and Chet, I. (2000). Induction and accumulation of PR proteins activityduring early stages of root colonizationby the mycoparasite Trichoderma harzianum strain T-203. Plant Physiology and Biochemistry 38, 863-873. DOI: https://doi.org/10.1016/S0981-9428(00)01198-0
Zandvakili, N., Zamani, M., Motallebi, M., and Jahromi, Z. M. (2017). Cloning, Overexpression and in vitro Antifungal Activity of Zea Mays PR10 Protein. Iranian journal of biotechnology 15, 42. DOI: https://doi.org/10.15171/ijb.1357
Zhou, J.-M. (1999). Signal transduction and pathogen-induced PR gene expression. Pathogenesis-related proteins in plants, 195-205. DOI: https://doi.org/10.1201/9781420049299.ch9
Zhu, B., Chen, T. H., and H. Li, P. (1996). "Analysis of late-blight disease resistance and freezing tolerance in transgenic potato plants expressing sense and antisense genes for osmotin-like protein." DOI: https://doi.org/10.1007/BF00197588
Ziadi, S., Barbedette, S., Godard, J., Monot, C., Le Corre, D., and Silue, D. (2001). Production of pathogenesis‐related proteins in the cauliflower (Brassica oleracea var. botrytis)–downy mildew (Peronospora parasitica) pathosystem treated with acibenzolar‐S‐methyl. Plant Pathology 50, 579-586. DOI: https://doi.org/10.1046/j.1365-3059.2001.00609.x
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