UNDERSTANDING INVASIVE PLANT MYCOPARASITES AND THEIR REMEDY THROUGH ADVANCED MOLECULAR APPROACHES

Aqsa Parvaiz, Ghulam Mustafa, Faiz A. Joyia

Abstract


Fungi are historically notorious pests that have threatened availability of quality food. Several invasive species have appeared to be destructive for valuable crop species and even led to famine in certain severe cases. Surveillance and eradication of these disastrous microbial invaders is dependent on their sentinel behavior. Molecular Biology has helped to great extent in understanding these epidemic agents. Plant defense system as well as plant microbe interaction have well been explored and proved quite fruitful in understanding metabolic pathways involved in pathogenesis and defense response. Ultimately, researchers are able to define strategies for the control of these invasive pathogens. Genome editing has successfully been employed to develop pathogen resistant crops. Antifungal proteins have been expressed through transgenic technology to develop disease resistant plants. A few have proved to be the real success stories whereas others are at the stage of infancy. This review is an update about research work accomplished to-date, for the characterization and identification of fungal pathogens, metabolic pathways activated during plant pathogen interaction, advancements in the detection of fungal pathogens and transgenic plants developed to withstand pathogen attack.


Keywords


Invasive fungal pathogens, Plant defense response, Molecular diagnosis, Transgenics, Cisgenic approaches.

Full Text:

PDF

References


Adams, D. J. 2004. Fungal cell wall chitinases and glucanases. Microbiology, 150: 2029-2035.

Adie, B. A. T., J. Perez-Perez, M. M. Perez-Perez, M. Godoy, J. J. Sanchez-Serrano, E. A. Schmelz and R. Solano. 2007. ABA Is an Essential Signal for Plant Resistance to Pathogens Affecting JA Biosynthesis and the Activation of Defenses in Arabidopsis. The Plant Cell Online, 19: 1665-1681.

Albersheim, P. and A. J. Anderson. 1971. Proteins from Plant Cell Walls Inhibit Polygalacturonases Secreted by Plant Pathogens. Proceedings of the National Academy of Sciences, 68: 1815-1819.

Alexander, D., R. M. Goodman, M. Gut-Rella, C. Glascock, K. Weymann, L. Friedrich, D. Maddox, P. Ahl-Goy, T. Luntz and E. Ward. 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.

Amian, A. A., J. Papenbrock, H.-J. Jacobsen and F. Hassan. 2011. Enhancing transgenic pea (Pisum sativum L.) resistance against fungal diseases through stacking of two antifungal genes (chitinase and glucanase). GM crops, 2: 104-109.

Arshad, W., I.-u. Haq, M. T. Waheed, K. S. Mysore and B. Mirza. 2014. Agrobacterium-Mediated Transformation of Tomato with rolB Gene Results in Enhancement of Fruit Quality and Foliar Resistance against Fungal Pathogens. PLoS ONE, 9: e96979.

Baker, C. J. and E. W. Orlandi. 1995. Active Oxygen in Plant Pathogenesis. Annual Review of Phytopathology, 33: 299-321.

Bari, R. and J. D. G. Jones. 2008. Role of plant hormones in plant defence responses. Plant Molecular Biology, 69: 473-488.

Barna, B., J. Fodor, B. D. Harrach, M. Pogány and Z. Király. 2012. The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens. Plant Physiology and Biochemistry, 59: 37-43.

Bartnicki-Garcia, S. 1968. Cell Wall Chemistry, Morphogenesis, and Taxonomy of Fungi. Annual Review of Microbiology, 22: 87-108.

Beckers, G. J. M. and S. H. Spoel. 2006. Fine-Tuning Plant Defence Signalling: Salicylate versus Jasmonate. Plant Biology, 8: 1-10.

Bliffeld, M., J. Mundy, I. Potrykus and J. Fütterer. 1999. Genetic engineering of wheat for increased resistance to powdery mildew disease. Theoretical and Applied Genetics, 98: 1079-1086.

Broekaert, W. F., B. P. A. Cammue, M. F. C. De Bolle, K. Thevissen, G. W. De Samblanx, R. W. Osborn and K. Nielson. 1997. Antimicrobial Peptides from Plants. Critical Reviews in Plant Sciences, 16: 297-323.

Broekaert, W. F., J. Van Parijs, A. K. Allen and W. J. Peumans. 1988. Comparison of some molecular, enzymatic and antifungal properties of chitinases from thorn-apple, tobacco and wheat. Physiological and Molecular Plant Pathology, 33: 319-331.

Brogue, K., I. Chet, M. Holliday, R. Cressman, P. Biddle, S. Knowlton, C. J. Mauvais and R. Broglie. 1991. Transgenic Plants with Enhanced Resistance to the Fungal Pathogen Rhizoctonia solani. Science, 254: 1194-1197.

Cervone, F., G. De Lorenzo, L. Degrà and G. Salvi. 1986. Interaction of Fungal Polygalacturonase with Plant Proteins in Relation to Specificity and Regulation of Plant Defense Response. Recognition in Microbe-Plant Symbiotic and Pathogenic Interactions. Springer Berlin Heidelberg, pp. 253-258.

Chen, S. C., A. R. Liu and Z. R. Zou. 2006. Overexpression of glucanase gene and defensin gene in transgenic tomato enhances resistance to Ralstonia solanacearum. Russian Journal of Plant Physiology, 53: 671-677.

Chye, M.-L., K.-J. Zhao, Z.-M. He, S. Ramalingam and K.-L. Fung. 2004. An agglutinating chitinase with two chitin-binding domains confers fungal protection in transgenic potato. Planta, 220: 717-730.

Coca, M., C. Bortolotti, M. Rufat, G. Peñas, R. Eritja, D. Tharreau, A. M. del Pozo, J. Messeguer and B. San Segundo. 2004. Transgenic Rice Plants Expressing the Antifungal AFP Protein from Aspergillus Giganteus Show Enhanced Resistance to the Rice Blast Fungus Magnaporthe Grisea. Plant Molecular Biology, 54: 245-259.

Coca, M., G. Peñas, J. Gómez, S. Campo, C. Bortolotti, J. Messeguer and B. S. Segundo. 2005. Enhanced resistance to the rice blast fungus Magnaporthe grisea conferred by expression of a cecropin a gene in transgenic rice. Planta, 223: 392-406.

Couch, B. C., I. Fudal, M.-H. Lebrun, D. Tharreau, B. Valent, P. van Kim, J.-L. Nottéghem and L. M. Kohn. 2005. Origins of Host-Specific Populations of the Blast Pathogen Magnaporthe oryzae in Crop Domestication With Subsequent Expansion of Pandemic Clones on Rice and Weeds of Rice. Genetics, 170: 613-630.

Datta, K., J. Tu, N. Oliva, I. Ona, R. Velazhahan, T. W. Mew, S. Muthukrishnan and S. K. Datta. 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.

De Vos, M., V. R. Van Oosten, R. M. P. Van Poecke, J. A. Van Pelt, M. J. Pozo, M. J. Mueller, A. J. Buchala, J.-P. Métraux, L. C. Van Loon, M. Dicke and C. M. J. Pieterse. 2005. Signal signature and transcriptome changes of arabidopsis during pathogen and insect attack. Molecular Plant-Microbe Interactions, 18: 923-937.

De Wit, P. J. G. M. 2007. How plants recognize pathogens and defend themselves. Cellular and Molecular Life Sciences, 64: 2726-2732.

Dean, R., J. A. L. Van Kan, Z. A. Pretorius, K. E. Hammond-Kosack, A. Di Pietro, P. D. Spanu, J. J. Rudd, M. Dickman, R. Kahmann, J. Ellis and G. D. Foster. 2012. The Top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology, 13: 414-430.

Du, J., E. Verzaux, A. Chaparro-Garcia, G. Bijsterbosch, L. C. P. Keizer, J. Zhou, T. W. H. Liebrand, C. Xie, F. Govers, S. Robatzek, E. A. G. van der Vossen, E. Jacobsen, R. G. F. Visser, S. Kamoun and V. G. A. A. Vleeshouwers. 2015. Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nature Plants, 1: 15034.

Epple, P. 1997. Overexpression of an Endogenous Thionin Enhances Resistance of Arabidopsis against Fusarium oxysporum. The Plant Cell Online, 9: 509-520.

Fisher, M. 2012. emerging fungal threats to animal, plant and ecosystem health: c8-2. Mycoses, 55: 79-80.

Fisher, M. C., D. A. Henk, C. J. Briggs, J. S. Brownstein, L. C. Madoff, S. L. McCraw and S. J. Gurr. 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature, 484: 186-194.

Gao, A.-G., S. M. Hakimi, C. A. Mittanck, Y. Wu, B. M. Woerner, D. M. Stark, D. M. Shah, J. Liang and C. M. T. Rommens. 2000. Fungal pathogen protection in potato by expression of a plant defensin peptide. Nature Biotechnology, 18: 1307-1310.

Gaspar, Y. M., J. A. McKenna, B. S. McGinness, J. Hinch, S. Poon, A. A. Connelly, M. A. Anderson and R. L. Heath. 2014. Field resistance to Fusarium oxysporum and Verticillium dahliae in transgenic cotton expressing the plant defensin NaD1. Journal of Experimental Botany, 65: 1541-1550.

Ghosh, S., K. A. Molla, S. Karmakar, S. K. Datta and K. Datta. 2016. Enhanced resistance to late blight pathogen conferred by expression of rice oxalate oxidase 4 gene in transgenic potato. Plant Cell, Tissue and Organ Culture (PCTOC), 126: 429-437.

Grant, M. and C. Lamb. 2006. Systemic immunity. Current Opinion in Plant Biology, 9: 414-420.

Green, J. R., N. A. Pain, M. E. Cannell, C. P. Leckie, S. McCready, A. J. Mitchell, J. A. Callow, G. L. Jones, R. J. O'Connell and K. Mendgen. 1995. Analysis of differentiation and development of the specialized infection structures formed by biotrophic fungal plant pathogens using monoclonal antibodies. Canadian Journal of Botany, 73: 408-417.

Grover, A. and R. Gowthaman. 2003. Strategies for development of fungus-resistant transgenic plants. Current Science, 84: 330-340.

Gururani, M. A. and S. W. Park. 2012. Engineered resistance against filamentous pathogens in Solanum tuberosum. Journal of General Plant Pathology, 78: 377-388.

Haas, B. J., S. Kamoun, M. C. Zody, R. H. Jiang, R. E. Handsaker, L. M. Cano, M. Grabherr, C. D. Kodira, S. Raffaele and T. Torto-Alalibo. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature, 461: 393.

Hassan, F., J. Meens, H.-J. Jacobsen and H. Kiesecker. 2009. A family 19 chitinase (Chit30) from Streptomyces olivaceoviridis ATCC 11238 expressed in transgenic pea affects the development of T. harzianum in vitro. Journal of Biotechnology, 143: 302-308.

Honée, G. 1999. Engineered resistance against fungal plant pathogens. European Journal of Plant Pathology, 105: 319-326.

Ignacimuthu, S. and S. A. Ceasar. 2012. Development of transgenic finger millet (Eleusine coracana (L.) Gaertn.) resistant to leaf blast disease. Journal of Biosciences, 37: 135-147.

Islam, A. 2008. Fungus Resistant Transgenic Plants: Strategies, Progress and Lessons Learnt. Plant Tissue Culture and Biotechnology, 16.

Jach, G., B. Gornhardt, J. Mundy, J. Logemann, E. Pinsdorf, R. Leah, J. Schell and C. Maas. 1995. Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. The Plant Journal, 8: 97-109.

Jach, G., B. Görnhardt, J. Mundy, J. Logemann, E. Pinsdorf, R. Leah, J. Schell and C. Maas. 1995. Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. The Plant Journal, 8: 97-109.

Jones, J. D. G. and J. L. Dangl. 2006. The plant immune system. Nature, 444: 323-329.

Jongedijk, E., H. Tigelaar, J. S. C. van Roekel, S. A. Bres-Vloemans, I. Dekker, P. J. M. van den Elzen, B. J. C. Cornelissen and L. S. Melchers. 1995. Synergistic activity of chitinases and β-1,3-glucanases enhances fungal resistance in transgenic tomato plants. Euphytica, 85: 173-180.

Jordan, I. K. 2009. Faculty of 1000 evaluation for Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. F1000 - Post-publication peer review of the biomedical literature. Faculty of 1000, Ltd.

Karmakar, S., K. A. Molla, P. K. Chanda, S. N. Sarkar, S. K. Datta and K. Datta. 2015. Green tissue-specific co-expression of chitinase and oxalate oxidase 4 genes in rice for enhanced resistance against sheath blight. Planta, 243: 115-130.

Keon, J., J. Antoniw, R. Carzaniga, S. Deller, J. L. Ward, J. M. Baker, M. H. Beale, K. Hammond-Kosack and J. J. Rudd. 2007. Transcriptional Adaptation of Mycosphaerella graminicolato Programmed Cell Death (PCD) of Its Susceptible Wheat Host. Molecular Plant-Microbe Interactions, 20: 178-193.

Khan, A., I. A. Nasir, B. Tabassum, K. Aaliya, M. Tariq and A. Q. Rao. 2016. Expression studies of chitinase gene in transgenic potato against Alternaria solani. Plant Cell, Tissue and Organ Culture (PCTOC), 128: 563-576.

Khan, R. S., N. A. Darwish, B. Khattak, V. O. Ntui, K. Kong, K. Shimomae, I. Nakamura and M. Mii. 2014. Retransformation of marker-free potato for enhanced resistance against fungal pathogens by pyramiding chitinase and wasabi defensin genes. Molecular Biotechnology, 56: 814-823.

Kolmer, J. A. 1996. Genetics of resistance to wheat leaf rust. Annual Review of Phytopathology, 34: 435-455.

Kumar, K. K., K. Poovannan, R. Nandakumar, K. Thamilarasi, C. Geetha, N. Jayashree, E. Kokiladevi, J. A. J. Raja, R. Samiyappan, D. Sudhakar and P. Balasubramanian. 2003. A high throughput functional expression assay system for a defence gene conferring transgenic resistance on rice against the sheath blight pathogen, Rhizoctonia solani. Plant Science, 165: 969-976.

Lane, B. G. 2000. Oxalate oxidases and differentiating surface structure in wheat: germins. Biochemical Journal, 349: 309-321.

Lee, W.-S., B. J. Devonshire, K. E. Hammond-Kosack, J. J. Rudd and K. Kanyuka. 2015. Deregulation of plant cell death through disruption of chloroplast functionality affects asexual sporulation of Zymoseptoria tritici on wheat. Molecular Plant-Microbe Interactions, 28: 590-604.

Lin, W., C. S. Anuratha, K. Datta, I. Potrykus, S. Muthukrishnan and S. K. Datta. 1995. Genetic Engineering of Rice for Resistance to Sheath Blight. Nature Biotechnology, 13: 686-691.

Liu, D., K. G. Raghothama, P. M. Hasegawa and R. A. Bressan. 1994. Osmotin overexpression in potato delays development of disease symptoms. Proceedings of the National Academy of Sciences, 91: 1888-1892.

Liu, M., Z.-x. Sun, J. Zhu, T. Xu, G. E. Harman and M. Lorito. 2004. Science Letters: Enhancing rice resistance to fungal pathogens by transformation with cell wall degrading enzyme genes fromTrichoderma atroviride. Journal of Zhejiang University Science, 5: 133-136.

Logemann, J., G. Jach, S. Logemann, R. Leah, G. Wolf, J. Mundy, A. Oppenheim, I. Chet and J. Schell. 1993. Expression of a Ribosome Inhibiting Protein (RIP) or a Bacterial Chitinase Leads to Fungal Resistance in Transgenic Plants. Developments in Plant Pathology. Springer Netherlands, pp. 446-448.

Logemann, J., G. Jach, H. Tommerup, J. Mundy and J. Schell. 1992. Expression of a Barley Ribosome-Inactivating Protein Leads to Increased Fungal Protection in Transgenic Tobacco Plants. Nature Biotechnology, 10: 305-308.

Mackintosh, C. A., D. F. Garvin, L. E. Radmer, S. J. Heinen and G. J. Muehlbauer. 2005. A model wheat cultivar for transformation to improve resistance to Fusarium Head Blight. Plant Cell Reports, 25: 313-319.

Magan, N., D. Aldred, K. Mylona and R. J. W. Lambert. 2010. Limiting mycotoxins in stored wheat. Food Additives & Contaminants: Part A, 27: 644-650.

Mao, B., X. Liu, D. Hu and D. Li. 2013. Co-expression of RCH10 and AGLU1 confers rice resistance to fungal sheath blight Rhizoctonia solani and blast Magnorpathe oryzae and reveals impact on seed germination. World Journal of Microbiology and Biotechnology, 30: 1229-1238.

Masoud, S. A., Q. Zhu, C. Lamb and R. A. Dixon. 1996. Constitutive expression of an inducible β-1,3-glucanase in alfalfa reduces disease severity caused by the oomycete pathogen Phytophthora megasperma f. sp. medicaginis, but does not reduce disease severity of chitin-containing fungi. Transgenic Research, 5: 313-323.

Michielse, C. B. and M. Rep. 2009. Pathogen profile update: Fusarium oxysporum. Molecular Plant Pathology, 10: 311-324.

Mondal, K. K., R. C. Bhattacharya, K. R. Koundal and S. C. Chatterjee. 2006. Transgenic Indian mustard Brassica juncea expressing tomato glucanase leads to arrested growth of Alternaria brassicae. Plant Cell Reports, 26: 247-252.

Munir, F., S. Hayashi, J. Batley, S. M. S. Naqvi and T. Mahmood. 2015. Germin-like protein 2 gene promoter from rice is responsive to fungal pathogens in transgenic potato plants. Functional & Integrative Genomics, 16: 19-27.

Muthukrishnan, S., G. H. Liang, H. N. Trick and B. S. Gill. 2001. Enhanced resistance to sheath blight by constitutive expression of infection-related rice chitinase in transgenic elite indica rice cultivars. Plant Cell, Tissue and Organ Culture, 64: 93-114.

Nakajima, H., T. Muranaka, F. Ishige, K. Akutsu and K. Oeda. 1997. Fungal and bacterial disease resistance in transgenic plants expressing human lysozyme. Plant Cell Reports, 16: 674-679.

Nakamura, Y., H. Sawada, S. Kobayashi, I. Nakajima and M. Yoshikawa. 1999. Expression of soybean b -1,3-endoglucanase cDNA and effect on disease tolerance in kiwifruit plants. Plant Cell Reports, 18: 527-532.

Nelson-Smith, D. 1993. Brighton Crop Protection Conference 1993—Weeds: Introduction. Crop Protection, 12: 555-559.

Nishiuchi, T., D. Masuda, H. Nakashita, K. Ichimura, K. Shinozaki, S. Yoshida, M. Kimura, I. Yamaguchi and K. Yamaguchi. 2006. Fusarium phytotoxin trichothecenes have an elicitor-like activity in Arabidopsis thaliana, but the activity differed significantly among their molecular species. Molecular Plant-Microbe Interactions, 19: 512-520.

Nishizawa, Y., M. Saruta, K. Nakazono, Z. Nishio, M. Soma, T. Yoshida, E. Nakajima and T. Hibi. 2003. Characterization of transgenic rice plants over-expressing the stress-inducible β-glucanase gene Gns1. Plant Molecular Biology, 51: 143-152.

Nucci, M. and E. Anaissie. 2007. Fusarium Infections in Immunocompromised Patients. Clinical Microbiology Reviews, 20: 695-704.

Oerke, E. C. 2005. Crop losses to pests. The Journal of Agricultural Science, 144: 31.

Oerke, E. C. and H. W. Dehne. 2004. Safeguarding production—losses in major crops and the role of crop protection. Crop Protection, 23: 275-285.

Orton, E. S., S. Deller and J. K. M. Brown. 2011. Mycosphaerella graminicola: from genomics to disease control. Molecular Plant Pathology, 12: 413-424.

Osusky, M., L. Osuska, R. E. Hancock, W. W. Kay and S. Misra. 2004. Transgenic Potatoes Expressing a Novel Cationic Peptide are Resistant to Late Blight and Pink Rot. Transgenic Research, 13: 181-190.

Ou, S. H. 1980. Pathogen Variability and Host Resistance in Rice Blast Disease. Annual Review of Phytopathology, 18: 167-187.

Paciolla, C., N. Dipierro, G. Mulè, A. Logrieco and S. Dipierro. 2004. The mycotoxins beauvericin and T-2 induce cell death and alteration to the ascorbate metabolism in tomato protoplasts. Physiological and Molecular Plant Pathology, 65: 49-56.

Pan, S.-Q., X.-S. Ye and J. Kuć. 1989. Direct detection of β-1,3-glucanase isozymes on polyacrylamide electrophoresis and isoelectrofocusing gels. Analytical Biochemistry, 182: 136-140.

Park, S. W., E. Kaimoyo, D. Kumar, S. Mosher and D. F. Klessig. 2007. Methyl Salicylate Is a Critical Mobile Signal for Plant Systemic Acquired Resistance. Science, 318: 113-116.

Peng, X.-L., W.-T. Xu, Y. Wang, K.-L. Huang, Z.-h. Liang, W.-w. Zhao and Y.-B. Luo. 2009. Mycotoxin Ochratoxin A-induced cell death and changes in oxidative metabolism of Arabidopsis thaliana. Plant Cell Reports, 29: 153-161.

Perfect, S. E., H. B. Hughes, R. J. O'Connell and J. R. Green. 1999. Colletotrichum: A Model Genus for Studies on Pathology and Fungal–Plant Interactions. Fungal Genetics and Biology, 27: 186-198.

Pretorius, Z. A., R. P. Singh, W. W. Wagoire and T. S. Payne. 2000. Detection of Virulence to Wheat Stem Rust Resistance Gene Sr31 in Puccinia graminis. f. sp. tritici in Uganda. Plant Disease, 84: 203-203.

Prusky, D. 1996. Pathogen quiescence in postharvest diseases. Annual Review of Phytopathology, 34: 413-434.

Reader, J. 2009. Potato: a history of the propitious esculent. Yale University Press.

Rutter, W. B., A. Salcedo, A. Akhunova, F. He, S. Wang, H. Liang, R. L. Bowden and E. Akhunov. 2017. Divergent and convergent modes of interaction between wheat and Puccinia graminis f. sp. tritici isolates revealed by the comparative gene co-expression network and genome analyses. BMC Genomics, 18.

Samanta, I. 2015. Classification of Fungi. Veterinary Mycology. Springer India, pp. 9-10.

Scholefield, P. and J. Morison. 2010. Assessment of economic cost of endemic pests and diseases on the Australian grape and wine industry. Grape and Wine Research and Development Corporation (GWRDC) project. Project number: GWR, 8.

Sela-Buurlage, M. B., A. S. Ponstein, S. A. Bres-Vloemans, L. S. Melchers, P. J. M. van den Elzen and B. J. C. Cornelissen. 1993. Only Specific Tobacco (Nicotiana tabacum) Chitinases and [beta]-1,3-Glucanases Exhibit Antifungal Activity. Plant Physiology, 101: 857-863.

Selin, C., T. R. de Kievit, M. F. Belmonte and W. G. D. Fernando. 2016. Elucidating the Role of Effectors in Plant-Fungal Interactions: Progress and Challenges. Frontiers in Microbiology, 7.

Simmons, C. R. 1994. The Physiology and Molecular Biology of Plant 1,3- -D-Glucanases and 1,3;1,4- -D-Glucanases. Critical Reviews in Plant Sciences, 13: 325-325.

Singh, R. P., H. M. William, J. Huerta-Espino and G. Rosewarne. 2004. Wheat rust in Asia: meeting the challenges with old and new technologies. Proceedings of the 4th international crop science congress. The Regional Institute Ltd Gosford, Australia.

Sridevi, G., C. Parameswari, N. Sabapathi, V. Raghupathy and K. Veluthambi. 2008. Combined expression of chitinase and β-1,3-glucanase genes in indica rice (Oryza sativa L.) enhances resistance against Rhizoctonia solani. Plant Science, 175: 283-290.

Tabei, Y., S. Kitade, Y. Nishizawa, N. Kikuchi, T. Kayano, T. Hibi and K. Akutsu. 1998. Transgenic cucumber plants harboring a rice chitinase gene exhibit enhanced resistance to gray mold (Botrytis cinerea ). Plant Cell Reports, 17: 159-164.

Thakur, M. and B. S. Sohal. 2013. Role of Elicitors in Inducing Resistance in Plants against Pathogen Infection: A Review. ISRN Biochemistry, 2013: 1-10.

Tohidfar, M., M. Mohammadi and B. Ghareyazie. 2005. Agrobacterium -mediated transformation of cotton (Gossypium hirsutum) using a heterologous bean chitinase gene. Plant Cell, Tissue and Organ Culture, 83: 83-96.

Turner, R. S. 2005. After the famine: Plant pathology, Phytophthora infestans, and the late blight of potatoes, 1845–1960. Historical Studies in the Physical and Biological Sciences, 35: 341-370.

Van Baarlen, P., E. J. Woltering, M. Staats and J. A. L. Van Kan. 2007. Histochemical and genetic analysis of host and non-host interactions of Arabidopsis with three Botrytis species: an important role for cell death control. Molecular Plant Pathology, 8: 41-54.

Van Loon, L. 1997. Induced resistance in plants and the role of pathogenesis-related proteins: a review. European Journal of Plant Pathology (Netherlands).

Vellicce, G. R., J. C. D. Ricci, L. Hernández and A. P. Castagnaro. 2006. Enhanced Resistance to Botrytis cinerea Mediated by the Transgenic Expression of the Chitinase Gene ch5B in Strawberry. Transgenic Research, 15: 57-68.

Vivier, E. and B. Malissen. 2005. Innate and adaptive immunity: specificities and signaling hierarchies revisited. Nature Immunology, 6: 17-21.

Voegele, R. T. and K. W. Mendgen. 2011. Nutrient uptake in rust fungi: how sweet is parasitic life? Euphytica, 179: 41-55.

Walker-Simmons, M., L. Hadwiger and C. A. Ryan. 1983. Chitosans and pectic polysaccharides both induce the accumulation of the antifungal phytoalexin pisatin in pea pods and antinutrient proteinase inhibitors in tomato leaves. Biochemical and Biophysical Research Communications, 110: 194-199.

Wally, O., J. Jayaraj and Z. Punja. 2008. Comparative resistance to foliar fungal pathogens in transgenic carrot plants expressing genes encoding for chitinase, β-1,3-glucanase and peroxidise. European Journal of Plant Pathology, 123: 331-342.

Wang, X., N. Jiang, J. Liu, W. Liu and G.-L. Wang. 2014. The role of effectors and host immunity in plant–necrotrophic fungal interactions. Virulence, 5: 722-732.

Wang, Y., A. P. Kausch, J. M. Chandlee, H. Luo, B. A. Ruemmele, M. Browning, N. Jackson and M. R. Goldsmith. 2003. Co-transfer and expression of chitinase, glucanase, and bar genes in creeping bentgrass for conferring fungal disease resistance. Plant Science, 165: 497-506.

Wu, G. 1995. Disease Resistance Conferred by Expression of a Gene Encoding H2O2-Generating Glucose Oxidase in Transgenic Potato Plants. The Plant Cell Online, 7: 1357-1368.

Yamamoto, T., H. Iketani, H. Ieki, Y. Nishizawa, K. Notsuka, T. Hibi, T. Hayashi and N. Matsuta. 2000. Transgenic grapevine plants expressing a rice chitinase with enhanced resistance to fungal pathogens. Plant Cell Reports, 19: 639-646.

Yoshida, K., V. J. Schuenemann, L. M. Cano, M. Pais, B. Mishra, R. Sharma, C. Lanz, F. N. Martin, S. Kamoun, J. Krause, M. Thines, D. Weigel and H. A. Burbano. 2013. Correction: The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine. eLife, 2.

Zhu, B., T. H. Chen and P. Li. 1996. Analysis of late-blight disease resistance and freezing tolerance in transgenic potato plants expressing sense and antisense genes for an osmotin-like protein. Planta, 198.

Zhu, H., X. Xu, G. Xiao, L. Yuan and B. Li. 2007. Enhancing disease resistances of Super Hybrid Rice with four antifungal genes. Science in China Series C: Life Sciences, 50: 31-39.

Zhu, Q., E. A. Maher, S. Masoud, R. A. Dixon and C. J. Lamb. 1994. Enhanced Protection Against Fungal Attack by Constitutive Co–expression of Chitinase and Glucanase Genes in Transgenic Tobacco. Nature Biotechnology, 12: 807-812.

Zhu, Y. J., R. Agbayani, M. C. Jackson, C. S. Tang and P. H. Moore. 2004. Expression of the grapevine stilbene synthase gene VST1 in papaya provides increased resistance against diseases caused by Phytophthora palmivora. Planta, 220: 241-250.

Zipfel, C. and G. Felix. 2005. Plants and animals: a different taste for microbes. Current Opinion in Plant Biology, 8: 353-360.

Zoubenko, O., F. Uckun, Y. Hur, I. Chet and N. Tumer. 1997. Plant resistance to fungal infection induced by nontoxic pokeweed antiviral protein mutants. Nature Biotechnology, 15: 992-996.




DOI: https://doi.org/10.33866/phytopathol.030.02.0452

Refbacks

  • There are currently no refbacks.


Copyright (c) 2018 Aqsa Parvaiz, Ghulam Mustafa, Faiz A. Joyia

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

      
   
Pakistan Journal of Phytopathological
ISSN: 1019-763X (Print), 2305-0284 (Online).
© 2013 Pak. J. Phytopathol. All rights reserved.