Transgenic expression of antifungal pathogenesis-related proteins against phytopathogenic fungi – 15 years of success

In: Israel Journal of Plant Sciences

ABSTRACT

Being sessile organisms, plants are continuously challenged by phytopathogenic fungi, contributing the largest share in loss due to plant disease. Plants naturally possess a well-developed and programmed protein-based defense system, capable of producing antimicrobial cationic peptides to ward off pathogen attack. Numerous genes encoding antifungal proteins have been isolated, cloned, sequenced and transgenically expressed against multiple phytopathogenic fungi successfully. Genetic engineering technology has been widely utilized to produce transgenic plants with enhanced resistance against pathogens. Pathogenesis-related proteins (PR-proteins) is a group of the most important inducible defense-related antifungal proteins, including defensins, thionins, osomtin-like proteins, thaumatin-like proteins, chitinases, glucanases, oxalate oxidase or oxalate oxidase-like proteins and lipid transfer proteins. Transgenic plants have been developed by imparting the artificial expression of genes encoding antifungal PR-proteins. The expression of transgenes belonging to a single group of PR-proteins or synergistic action of transgenes from different groups has greatly uplifted the level of defense response in plants against fungi. Transgenic expression of antifungal PR-proteins has led to remarkably enhanced resistance in transgenic plants. In this review, we have summarized the role of PR-proteins in plant defense against fungi and 15 years of success achieved so far to generate a variety of transgenic plants resistant against fungi through overexpression of transgenes from different groups of PR-proteins.

  • Abdallah NA, Shah D, Abbas D, Madkour M. 2010. Stable integration and expression of a plant defensin in tomato confers resistance to Fusarium wilt. GM Crops. 1:344–350.

    • Search Google Scholar
    • Export Citation
  • Acharya K, Pal AK, Gulati A, Kumar S, Singh AK, Ahuja PS. 2013. Overexpression of Camellia sinensis thaumatin-like protein, CsTLP in potato confers enhanced resistance to Macrophomina phaseolina and Phytophthora infestans infection. Mol Biotechnol. 54:609–622.

    • Search Google Scholar
    • Export Citation
  • Aghazadeh R, Zamani M, Motallebi M, Moradyar M, Jahromi ZM. 2016. Co-transformation of canola by chimeric chitinase and tlp. World J Microbiol. Biotechnol. 32:1–2.

    • Search Google Scholar
    • Export Citation
  • Ahuja I, Kissen R, Bones AM. 2012. Phytoalexins in defense against pathogens. Trends Plant Sci. 17:73–90.

  • Amian AA, Papenbrock J, Jacobsen HJ, Hassan F. 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.

    • Search Google Scholar
    • Export Citation
  • Anand A, Zhou T, Trick HN, Gill BS, Bockus WW, Muthukrishnan S. 2003. Greenhouse and field testing of transgenic wheat plants stably expressing genes for thaumatin-like protein, chitinase and glucanase against Fusarium graminearum. J Exp Bot. 54:1101–1111.

    • Search Google Scholar
    • Export Citation
  • Antoniw JF, Ritter CE, Pierpoint WS, van Loon LC. 1980. Comparison of three pathogenesis-related proteins from plants of two cultivars of tobacco infected with TMV. J Gen Virol. 47:79–87.

    • Search Google Scholar
    • Export Citation
  • Anuradha TS, Divya K, Jami SK, Kirti PB. 2008. Transgenic tobacco and peanut plants expressing a mustard defensin show resistance to fungal pathogens. Plant Cell Rep. 27:1777–1786.

    • Search Google Scholar
    • Export Citation
  • Bezirganoglu I, Hwang SY, Fang TJ, Shaw JF. 2013. Transgenic lines of melon (Cucumis melo L. var. makuwa cv. ‘Silver Light’) expressing antifungal protein and chitinase genes exhibit enhanced resistance to fungal pathogens. Plant Cell Tiss Org Cult (PCTOC). 112:227–237.

    • Search Google Scholar
    • Export Citation
  • Bohlmann H, Clausen S, Behnke S, Giese H, Hiller C, Reimann-Philipp U, Schrader G, Barkholt V, Apel K. 1988. Leaf-specific thionins of barley – a novel class of cell wall proteins toxic to plant-pathogenic fungi and possibly involved in the defence mechanism of plants. EMBO J. 7:1559–1565.

    • Search Google Scholar
    • Export Citation
  • Boller T. 1993. Antimicrobial functions of the plant hydrolases, chitinases and β-1,3-glucanases. In: Fritig B. Legrand M, editors. Mechanisms of plant defense responses. Dordrecht: Kluwer Academic Press; p. 391–400.

    • Search Google Scholar
    • Export Citation
  • Borad V, Sriram S. 2008. Pathogenesis-related proteins for the plant protection. Asian J Exp Sci. 22:189–196.

  • Broglie K, Chet I, Holliday M, Cressman R, Biddle R, Knowlton S, Mauvais CJ, Broglie R. 1991. Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science. 254:1194–1197.

    • Search Google Scholar
    • Export Citation
  • Bruix M, Jimenez MA, Santoro J, Gonzalez C, Colilla FJ, Mendez E, Rico M. 1993. Solution structure of gamma 1-H and gamma 1-P thionins from barley and wheat endosperm determined by 1H-NMR: a structural motif common to toxic arthropod proteins. Biochem. 32:715–724.

    • Search Google Scholar
    • Export Citation
  • Carter C, Graham RA, Thornburg RW. 1998. Arabidopsis thaliana contains a large family of germin-like proteins: characterization of cDNA and genomic sequences encoding 12 unique family members. Plant Mol Biol. 38:929–943.

    • Search Google Scholar
    • Export Citation
  • Castro MS, Fontes W. 2005. Plant defense and antimicrobial peptides. Prot Pept Lett. 12:13–18.

  • Ceasar SA, Ignacimuthu S. 2012. Genetic engineering of crop plants for fungal resistance: role of antifungal genes. Biotechnol Lett. 34:995–1002.

    • Search Google Scholar
    • Export Citation
  • Chan YL, Prasad V, Chen KH, Liu PC, Chan MT, Cheng CP. 2005. Transgenic tomato plants expressing an Arabidopsis thionin (Thi2. 1) driven by fruit-inactive promoter battle against phytopathogenic attack. Planta. 221:386–393.

    • Search Google Scholar
    • Export Citation
  • Chalavi V, Tabaeizadeh, Z, Thibodeau P. 2003. Enhanced resistance to Verticillium dahliae in transgenic strawberry plants expressing a Lycopersicon chilense chitinase gene. J Americ Soc Hort Sci. 128:747–753.

    • Search Google Scholar
    • Export Citation
  • Chassot C, Nawrath C, Metraux JP. 2007. Cuticular defects lead to full immunity to a major plant pathogen. Plant J. 49:972–980.

  • Chen JJ, Chen GH, Hsu HC, Li SS, Chen CS. 2004. Cloning and functional expression of a mungbean defensin VrD1 in Pichia pastoris. J Agric Food Chem. 52:2256–2261.

    • Search Google Scholar
    • Export Citation
  • Chhikara S, Chaudhury D, Dhankher OP, Jaiwal PK. 2012. Combined expression of a barley class II chitinase and type I ribosome inactivating protein in transgenic Brassica juncea provides protection against Alternaria brassicae. Plant Cell Tiss Org Cul (PCTOC). 108:83–89.

    • Search Google Scholar
    • Export Citation
  • Chriscoe SM. 2008. Characterization of transgenic peanuts expressing oxalate oxidase for governmental approval of their release for control of Sclerotinia blight [MSc dissertation]. Blacksburg, VA: Virginia Polytechnic Institute and State University.

    • Search Google Scholar
    • Export Citation
  • Chye ML, Zhao KJ, He ZM, Ramalingam S, Fung KL. 2005. An agglutinating chitinase with two chitin-binding domains confers fungal protection in transgenic potato. Planta. 220:717–730.

    • Search Google Scholar
    • Export Citation
  • Colilla FJ, Rocher A, Mendez E. 1990. γ-Purothionins: amino acid sequence of two polypeptides of a new family of thionins from wheat endosperm. FEBS Lett. 270:191–194.

    • Search Google Scholar
    • Export Citation
  • Dafny-Yelin M, Tzfira T. 2007. Delivery of multiple transgenes to plant cells. Plant Physiol. 145:1118–1128.

  • Das M, Chauhan H, Chhibbar A, Haq QMR, Khurana P. 2011. High-efficiency transformation and selective tolerance against biotic and abiotic stress in mulberry, Morus indica cv. K2, by constitutive and inducible expression of tobacco osmotin. Trans Res. 20:231–246.

    • Search Google Scholar
    • Export Citation
  • da Silva LF, Dias CV, Cidade LC, Mendes JS, Pirovani CP, Alvim FC, Pereira GA, Aragão FJ, Cascardo JC, Costa MG. 2011. Expression of an oxalate decarboxylase impairs the necrotic effect induced by Nep1-like protein (NLP) of Moniliophthora perniciosa in transgenic tobacco. Mol Plant-Microbe Interact. 24:839–848.

    • Search Google Scholar
    • Export Citation
  • Datta K, Velazhahan R, Oliva N, Ona I, Mew T, Khush GS, Muthukrishnan S, Datta SK. 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. Theor Appl Genet. 98:1138–1145.

    • Search Google Scholar
    • Export Citation
  • Datta K, Tu J, Oliva N, Ona I, Velazhahan R, Mew TW, Muthukrishnan S, Datta SK. 2001. Enhanced resistance to sheath blight by constitutive expression of infection-related rice chitinase in transgenic elite indica rice cultivars. Plant Sci. 160:405–414.

    • Search Google Scholar
    • Export Citation
  • de Cáceres González FFN, Davey MR, Sanchez EC, Wilson ZA. 2015. Conferred resistance to Botrytis cinerea in Lilium by overexpression of the RCH10 chitinase gene. Plant Cell Rep. 34:1201–1209.

    • Search Google Scholar
    • Export Citation
  • Dias BB, Cunha WG, Morais LS, Vianna GR, Rech EL, Capdeville GD, Aragão FJ. 2006. Expression of an oxalate decarboxylase gene from Flammulina sp. in transgenic lettuce (Lactuca sativa) plants and resistance to Sclerotinia sclerotiorum. Plant Pathol. 55:187–193.

    • Search Google Scholar
    • Export Citation
  • Donaldson PA, Anderson T, Lane BG, Davidson AL, Simmonds DH. 2001. Soybean plants expressing an active oligomeric oxalate oxidase from the wheat gf-2.8 (germin) gene are resistant to the oxalate-secreting pathogen Sclerotina sclerotiorum. Physiol Mol Plant Pathol. 59:297–307.

    • Search Google Scholar
    • Export Citation
  • Dong X, Ji R, Guo X, Foster SJ, Chen H, Dong C, Liu Y, Hu Q, Liu S. 2008. Expressing a gene encoding wheat oxalate oxidase enhances resistance to Sclerotinia sclerotiorum in oilseed rape (Brassica napus). Planta. 228:331–340.

    • Search Google Scholar
    • Export Citation
  • Dunwell JM, Khuri S, Gane PJ. 2000. Microbial relatives of the seed storage proteins of higher plants: conservation of structure and diversification of function during evolution of the cupin superfamily. Microbiol Mol Biol Rev. 64:153–179.

    • Search Google Scholar
    • Export Citation
  • Dunwell JM, Gibbings JG, Mahmood T, Naqvi SMS. 2008. Germin and germin-like proteins: evolution, structure, and function. Crit Rev Plant Sci. 27:342–375.

    • Search Google Scholar
    • Export Citation
  • Durrant WE, Dong X. 2004. Systemic acquired resistance. Annu Rev Phytopathol. 42:185–209.

  • Dutton MV, Evans CS. 1996. Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment. Canad J Microbiol. 42:881–895.

    • Search Google Scholar
    • Export Citation
  • Epple P, Apel K, Bohlmann H. 1995. An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol. 109:813–820.

    • Search Google Scholar
    • Export Citation
  • Fagoaga C, Rodrigo I, Conejero V, Hinarejos C, Tuset JJ, Arnau J, Pina JA, Navarro L, Peña L. 2001. Increased tolerance to Phytophthora citrophthora in transgenic orange plants constitutively expressing a tomato pathogenesis related protein PR-5. Mol Breed. 7:175–185.

    • Search Google Scholar
    • Export Citation
  • Fang WE, Jie HU, Yan YA, Hao ZD, Wu RH, Tian BM, Cao GQ, Xin ZA. 2015. Transgenic Arabidopsis thaliana expressing a wheat oxalate oxidase exhibits hydrogen peroxide related defense response. J Integrat Agric. 14:2565–2573.

    • Search Google Scholar
    • Export Citation
  • Ferreira RB, Monteiro S, Freitas R, Santos CN, Chen Z, Batista LM, Duarte J, Borges A, Teixeira AR. 2007. The role of plant defense proteins in fungal pathogenesis. Mol Plant Pathol. 8:677–700.

    • Search Google Scholar
    • Export Citation
  • Fierens E, Rombouts S, Gebruers K, Goesaert H, Brijs K, Beaugrand J, Volckaert G, Van Campenhout S, Proost P, Courtin CM, Delcour JA. 2007. TLXI, a novel type of xylanase inhibitor from wheat (Triticum aestivum) belonging to the thaumatin family. Biochem J. 403:583–591.

    • Search Google Scholar
    • Export Citation
  • Filipenko EA, Kochetov AV, Kanayama Y, Malinovsky VI, Shumny VK. 2013. PR-proteins with ribonuclease activity and plant resistance against pathogenic fungi. Russ J Genet Appl Res. 3:474–480.

    • Search Google Scholar
    • Export Citation
  • François IE, Broekaert WF, Cammue BP. 2002. Different approaches for multi-transgene-stacking in plants. Plant Sci. 163:281–295.

  • Fu D, Tisserat NA, Xiao Y, Settle D, Muthukrishnan S, Liang GH. 2005. Overexpression of rice TLPD34 enhances dollar-spot resistance in transgenic bentgrass. Plant Sci. 168:671–680.

    • Search Google Scholar
    • Export Citation
  • Fujimori N, Enoki S, Suzuki A, Naznin HA, Shimizu M, Suzuki S. 2016. Grape apoplasmic β-1, 3-glucanase confers fungal disease resistance in Arabidopsis. Sci Horti. 200:105–110.

    • Search Google Scholar
    • Export Citation
  • Garcı´a-Olmedo F, Molina A, Segura A, Moreno M. 1995. The defensive role of nonspecific lipid-transfer proteins in plants. Trends Microbiol. 3:72–74.

    • Search Google Scholar
    • Export Citation
  • Gaspar YM, McKenna JA, McGinness BS, Hinch J, Poon S, Connelly AA, Anderson MA, Heath RL. 2014. Field resistance to Fusarium oxysporum and Verticillium dahliae in transgenic cotton expressing the plant defensin NaD1. J Exp Bot. 65:1541–1550.

    • Search Google Scholar
    • Export Citation
  • George A. 2014. An investigation into the potential of oxalate decarboxylase enzyme, to confer tolerance to Sclerotium cepivorum in transgenic Alliums [doctoral dissertation]. Christchurch: Lincoln University.

    • Export Citation
  • Ghag SB, Shekhawat UKS, Ganapathi TR. 2012. Petunia floral defensins with unique prodomains as novel candidates for development of Fusarium wilt resistance in transgenic banana plants. PLoS One. 7:e39557.

    • Search Google Scholar
    • Export Citation
  • Girhepuje PV, Shinde GB. 2011. Transgenic tomato plants expressing a wheat endochitinase gene demonstrate enhanced resistance to Fusarium oxysporum f. sp. lycopersici. Plant Cell Tiss Org Cult (PCTOC). 105:243–251.

    • Search Google Scholar
    • Export Citation
  • Green TR, Ryan CA. 1972. Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science. 175:776–777.

    • Search Google Scholar
    • Export Citation
  • Gurr SJ, Rushton PJ. 2005. Engineering plants with increased disease resistance: what are we going to express? TRENDS Biotechnol. 23:275–282.

    • Search Google Scholar
    • Export Citation
  • Halpin C, Boerjan W. 2003. Stacking transgenes in forest trees. Trends Plant Sci. 8:363–365.

  • Hammond-Kosack KE, Jones JDG. 1996. Inducible plant defense mechanisms and resistance gene function. Plant Cell. 8:1773–1791.

  • He X, Miyasaka SC, Fitch MM, Moore PH, Zhu YJ. 2008. Agrobacterium tumefaciens-mediated transformation of taro (Colocasia esculenta (L.) Schott) with a rice chitinase gene for improved tolerance to a fungal pathogen Sclerotium rolfsii. Plant Cell Rep. 27:903–909.

    • Search Google Scholar
    • Export Citation
  • He X, Miyasaka SC, Fitch MM, Khuri S, Zhu YJ. 2013. Taro (Colocasia esculenta) transformed with a wheat oxalate oxidase gene for improved resistance to taro pathogen Phytophthora colocasiae. Hort Sci. 48:22–27.

    • Search Google Scholar
    • Export Citation
  • Honee G. 1999. Engineered resistance against fungal plant pathogens. Eur J Plant Pathol. 105:319–326.

  • Hoshikawa K, Ishihara G, Takahashi H, Nakamura I. 2012. Enhanced resistance to gray mold (Botrytis cinerea) in transgenic potato plants expressing thionin genes isolated from Brassicaceae species. Plant Biotechnol. 29:87–93.

    • Search Google Scholar
    • Export Citation
  • Hou MM, Xu WJ, Bai H, Liu YM, Li LY. 2012. Characteristic expression of rice pathogenesis-related proteins in rice leaves during interactions with Xanthomonas oryzae pv. oryzae. Plant Cell Rep. 31:895–904.

    • Search Google Scholar
    • Export Citation
  • Huang Y, Liu H, Jia Z, Fang Q, Luo K. 2012. Combined expression of antimicrobial genes (Bbchit1 and LJAMP2) in transgenic poplar enhances resistance to fungal pathogens. Tree Physiol. 32:1313–1320.

    • Search Google Scholar
    • Export Citation
  • Huang X, Wang J, Du Z, Zhang C, Li L, Xu Z. 2013. Enhanced resistance to stripe rust disease in transgenic wheat expressing the rice chitinase gene RC24. Trans Res. 22:939–947.

    • Search Google Scholar
    • Export Citation
  • Ignacimuthu S, Ceasar SA. 2012. Development of transgenic finger millet (Eleusine coracana (L.) Gaertn.) resistant to leaf blast disease. J Biosci. 37:135–147.

    • Search Google Scholar
    • Export Citation
  • Jacobs AS, Pretorius ZA, Kloppers FJ, Cox TS. 1996. Mechanisms associated with wheat leaf rust resistance derived from Triticum monococcum. Phytopathology. 86:588–595.

    • Search Google Scholar
    • Export Citation
  • Jayaraj J, Muthukrishnan S, Liang GH, Velazhahan R. 2004. Jasmonic acid and salicylic acid induce accumulation of β-1,3-glucanase and thaumatin-like proteins in wheat and enhance resistance against Stagonospora nodorum. Biol Plantarum. 48:425–430.

    • Search Google Scholar
    • Export Citation
  • Jayaraj J, Punja ZK. 2007. Combined expression of chitinase and lipid transfer protein genes in transgenic carrot plants enhances resistance to foliar fungal pathogens. Plant Cell Rep. 26:1539–1546.

    • Search Google Scholar
    • Export Citation
  • Jha S, Chattoo BB. 2010. Expression of a plant defensin in rice confers resistance to fungal phytopathogens. Trans Res. 19:373–384.

  • Jiang L, Wu J, Fan S, Li W, Dong L, Cheng Q, Xu P, Zhang S. 2015. Isolation and characterization of a novel pathogenesis-related protein gene (GmPRP) with induced expression in soybean (Glycine max) during infection with Phytophthora sojae. PLoS one. 10:e0129932.

    • Search Google Scholar
    • Export Citation
  • Joshi RK, Nayak S. 2010. Gene pyramiding – a broad spectrum technique for developing durable stress resistance in crops. Biotechnol Mol Biol Rev. 5:51–60.

    • Search Google Scholar
    • Export Citation
  • Kader JC. 1975. Proteins and the intracellular exchange of lipids. I. Stimulation of phospholipids exchange between mitochondria and microsomal fractions by proteins isolated from potato tuber. Biochem Biophys Acta. 380:31–44.

    • Search Google Scholar
    • Export Citation
  • Kader JC. 1996. Lipid-transfer proteins in plants. Annu Rev Plant Physiol Plant Mol Biol. 47:627–654.

  • Kalpana K, Maruthasalam S, Rajesh T, Poovannan K, Kumar KK, Kokiladevi E, Raja JA, Sudhakar D, Velazhahan R, Samiyappan R, Balasubramanian P. 2006. Engineering sheath blight resistance in elite indica rice cultivars using genes encoding defense proteins. Plant Sci. 170:203–215.

    • Search Google Scholar
    • Export Citation
  • Kanzaki H, Nirasawa S, Saitoh H, Ito M, Nishihara M, Terauchi R, Nakamura I. 2002. Overexpression of the wasabi defensin gene confers enhanced resistance to blast fungus (Magnaporthe grisea) in transgenic rice. Theor Appl Genet. 105:809–814.

    • Search Google Scholar
    • Export Citation
  • Kasprzewska A. 2003. Plant chitinases – regulation and function. Cell Mol Biol Lett. 8:809–824.

  • Karmakar S, Molla KA, Chanda PK, Sarkar SN, Datta SK, Datta K. 2016. Green tissue-specific co-expression of chitinase and oxalate oxidase 4 genes in rice for enhanced resistance against sheath blight. Planta. 243:115–130.

    • Search Google Scholar
    • Export Citation
  • Kaur J, Fellers J, Adholeya A, Velivelli SL, El-Mounadi K, Nersesian N, Clemente T, Shah D. 2016. Expression of apoplast-targeted plant defensin MtDef4. 2 confers resistance to leaf rust pathogen Puccinia triticina but does not affect mycorrhizal symbiosis in transgenic wheat. Trans Res. 1–3.

    • Search Google Scholar
    • Export Citation
  • Keishiro WA, Ozaki Y, Matsubara H, Yoshizumi H. 1982. Studies on purothionin by chemical modifications. J Biochem. 91:257–63.

  • Kern MF, de Faria Maraschin S, Vom Endt D, Schrank A, Vainstein MH, Pasquali G. 2010. Expression of a chitinase gene from Metarhizium anisopliae in tobacco plants confers resistance against Rhizoctonia solani. Appl Biochem Biotechnol. 160:1933–1946.

    • Search Google Scholar
    • Export Citation
  • Kesarwani M, Azam M, Natarajan K, Mehta A, Datta A. 2000. Oxalate decarboxylase from Collybia velutipes molecular cloning and its overexpression to confer resistance to fungal infection in transgenic tobacco and tomato. J Biol Chem. 275:7230–7238.

    • Search Google Scholar
    • Export Citation
  • Khan RS, Nishihara M, Yamamura S, Nakamura I, Mii M. 2006. Transgenic potatoes expressing wasabi defensin peptide confer partial resistance to gray mold (Botrytis cinerea). Plant Biotechnol. 23:179–183.

    • Search Google Scholar
    • Export Citation
  • Kim JK, Jang IC, Wu R, Zuo WN, Boston RS, Lee YH, Ahn IP, Nahm BH. 2003. Co-expression of a modified maize ribosome-inactivating protein and a rice basic chitinase gene in transgenic rice plants confers enhanced resistance to sheath blight. Trans Res. 12:475–484.

    • Search Google Scholar
    • Export Citation
  • Kishimoto K, Nishizawa Y, Tabei Y, Hibi T, Nakajima M, Akutsu K. 2002. Detailed analysis of rice chitinase gene expression in transgenic cucumber plants showing different levels of disease resistance to gray mold (Botrytis cinerea). Plant Sci. 162:655–662.

    • Search Google Scholar
    • Export Citation
  • Kitajima S, Sato F. 1999. Plant pathogenesis-related proteins: molecular mechanisms of gene expression and protein function. J Biochem. 125:1–8.

    • Search Google Scholar
    • Export Citation
  • Koiwa H, Kato H, Nakatsu T, Oda J, Sato F. 1997. Purification and characterization of tobacco pathogenesis-related protein PR-5d, an antifungal thaumatin like protein. Plant Cell Physiol. 38:783–791.

    • Search Google Scholar
    • Export Citation
  • Kovács G, Sági L, Jacon G, Arinaitwe G, Busogoro JP, Thiry E, Strosse H, Swennen R, Remy S. 2013. Expression of a rice chitinase gene in transgenic banana (‘Gros Michel’, AAA genome group) confers resistance to black leaf streak disease. Trans Res. 22:117–130.

    • Search Google Scholar
    • Export Citation
  • Kravchik M, Bernstein N. 2013. Effects of salinity on the transcriptome of growing maize leaf cells points at differential involvement of the antioxidative response in cell growth restriction. BMC Genomics. 16:14:24.

    • Search Google Scholar
    • Export Citation
  • Krebitz M, Wagner B, Ferreira F, Peterbauer C, Campillo N, Witty M, Kolarich D, Steinkellner H, Scheiner O, Breiteneder H. 2003. Plant-based heterologous expression of Mal d 2, a thaumatin-like protein and allergen of apple (Malus domestica), and its characterization as an antifungal protein. J Mol Biol. 329:721–730.

    • Search Google Scholar
    • Export Citation
  • Lacerda AF, Del Sarto RP, Silva MS, de Vasconcelos EA, Coelho RR, dos Santos VO, Godoy CV, Seixas CD, da Silva MC, Grossi-de-Sa MF. 2016. The recombinant pea defensin Drr230a is active against impacting soybean and cotton pathogenic fungi from the genera Fusarium, Colletotrichum and Phakopsora. Biotechnology. 6:1–0.

    • Search Google Scholar
    • Export Citation
  • Lagrimini LM, Burkhart W, Moyer M, Rothstein S. 1987. Molecular cloning of complementary DNA encoding the lignin-forming peroxidase from tobacco: molecular analysis and tissue-specific expression. Proc Natl Acad Sci USA. 84:7542–7546.

    • Search Google Scholar
    • Export Citation
  • Lane B. 1994. Oxalate, germin, and the extracellular matrix of higher plants. FASEB J. 8:294–301.

  • Lane BG, Dunwell JM, Ray JA, Schmitt MR, Cuming AC. 1993. Germin, a protein marker of early plant development, is an oxalate oxidase. J Biol Chem. 268:12239–12242.

    • Search Google Scholar
    • Export Citation
  • Lee HI, Raikel NV. 1995. Prohevein is poorly processed but shows enhanced resistance to a chitin-binding fungus in transgenic tomato plants. Braz J Med Biol Res. 28:743–750.

    • Search Google Scholar
    • Export Citation
  • Li Z, Zhou M, Zhang Z, Ren L, Du L, Zhang B, Xu H, Xin Z. 2011. Expression of a radish defensin in transgenic wheat confers increased resistance to Fusarium graminearum and Rhizoctonia cerealis. Funct Integ Genom. 11:63–70.

    • Search Google Scholar
    • Export Citation
  • Li X, Gasic K, Cammue B, Broekaert W, Korban SS. 2003. Transgenic rose lines harboring an antimicrobial protein gene, Ace-AMP1, demonstrate enhanced resistance to powdery mildew (Sphaerotheca pannosa). Planta. 218:226–232.

    • Search Google Scholar
    • Export Citation
  • Li HY, Zhu YM, Chen Q, Conner RL, Ding XD, Li J, Zhang BB. 2004. Production of transgenic soybean plants with two anti-fungal protein genes via Agrobacterium and particle bombardment. Biol Plantar. 48:367–374.

    • Search Google Scholar
    • Export Citation
  • Liang H, Maynard CA, Allen RD, Powell WA. 2001. Increased Septoria musiva resistance in transgenic hybrid poplar leaves expressing a wheat oxalate oxidase gene. Plant Mol Biol. 45:619–629.

    • Search Google Scholar
    • Export Citation
  • Liu YJ, Cheng CS, Lai SM, Hsu MP, Chen CS, Lyu PC. 2006. Solution structure of the plant defensin VrD1 from mung bean and its possible role in insecticidal activity against bruchids. Prot Struc Funct Bioinfor. 63:777–786.

    • Search Google Scholar
    • Export Citation
  • Liu D, He X, Li W, Chen C, Ge F. 2012. Molecular cloning of a thaumatin-like protein gene from Pyrus pyrifolia and overexpression of this gene in tobacco increased resistance to pathogenic fungi. Plant Cell Tiss Org Cul (PCTOC). 111:29–39.

    • Search Google Scholar
    • Export Citation
  • Liu F, Wang M, Wen J, Yi B, Shen J, Ma C, Tu J, Fu T. 2015. Overexpression of barley oxalate oxidase gene induces partial leaf resistance to Sclerotinia sclerotiorum in transgenic oilseed rape. Plant Pathol. 64:1407–1416.

    • Search Google Scholar
    • Export Citation
  • Livingstone DM, Hampton JL, Phipps PM, Grabau EA. 2005. Enhancing resistance to Sclerotinia minor in peanut by expressing a barley oxalate oxidase gene. Plant Physiol. 137:1354–1362.

    • Search Google Scholar
    • Export Citation
  • Mahdavi F, Sariah M, Maziah M. 2012. Expression of rice thaumatin-like protein gene in transgenic banana plants enhances resistance to Fusarium wilt. Appl Biochem Biotechnol. 166:1008–1019.

    • Search Google Scholar
    • Export Citation
  • Mackintosh CA, Lewis J, Radmer LE, Shin S, Heinen SJ, Smith LA, Wyckoff MN, Dill-Macky R, Evans CK, Kravchenko S, Baldridge GD. 2007. Overexpression of defense response genes in transgenic wheat enhances resistance to Fusarium head blight. Plant Cell Rep. 26:479–488.

    • Search Google Scholar
    • Export Citation
  • Maximova SN, Marelli JP, Young A, Pishak S, Verica JA, Guiltinan MJ. 2006. Over-expression of a cacao class I chitinase gene in Theobroma cacao L. enhances resistance against the pathogen, Colletotrichum gloeosporioides. Planta. 224:740–749.

    • Search Google Scholar
    • Export Citation
  • Melander M, Kamnert I, Happstadius I, Liljeroth E, Bryngelsson T. 2006. Stability of transgene integration and expression in subsequent generations of doubled haploid oilseed rape transformed with chitinase and β-1, 3-glucanase genes in a double-gene construct. Plant Cell Rep. 25:942–952.

    • Search Google Scholar
    • Export Citation
  • Melchers LS, Stuiver MH. 2000. Novel genes for disease resistance breeding. Curr Opin Plant Biol. 3:147–152.

  • Melchers LS, Apotheker-de Groot M, Van der Knaap JA, Ponstein AS, Sela-Buurlage MB, Bol JF, Cornelissen BJC, Van den Elzen PJM, Linthorst HJM. 1994. A new class of tobacco chitinases homologous to bacterial exo-chitinases displays antifungal activity. Plant J. 5:469–480.

    • Search Google Scholar
    • Export Citation
  • Mendez E, Moreno A, Colilla F, Pelaez F, Limas GG, Mendez R, Soriano F, Salinas M, de Haro C. 1990. Primary structure and inhibition of protein synthesis in eukaryotic cell-free system of a novel thionin, gamma-hordothionin, from barley endosperm. Eur J Biochem. 194:533–539.

    • Search Google Scholar
    • Export Citation
  • Métraux JP, Streit L, Staub T. 1988. A pathogenesis-related protein in cucumber is a chitinase. Physiol Mol Plant Pathol. 33:1–9.

  • M'hamdi M, Chikh-Rouhou H, Boughalleb N, de Galarreta IR. 2012. Enhanced resistance to Rhizoctonia solani by combined expression of chitinase and Ribosome Inactivating Protein in transgenic potatoes (Solanum tuberosum L.). Spanish J Agric Res. 3:778–85.

    • Search Google Scholar
    • Export Citation
  • Misra RC, Sandeep MK, Kumar S, Ghosh S. 2016. A thaumatin-like protein of Ocimum basilicum confers tolerance to fungal pathogen and abiotic stress in transgenic Arabidopsis. Sci Rep. 6:25340. doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Mindrinos M, Katagiri F, Yu GL, Ausubel FM. 1994. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell. 78:1089–1099.

    • Search Google Scholar
    • Export Citation
  • Molla KA, Karmakar S, Chanda PK, Ghosh S, Sarkar SN, Datta SK, Datta K. 2013. Rice oxalate oxidase gene driven by green tissue–specific promoter increases tolerance to sheath blight pathogen (Rhizoctonia solani) in transgenic rice. Mol Plant Pathol. 14:910–22.

    • Search Google Scholar
    • Export Citation
  • Mondal KK, Bhattacharya RC, Koundal KR, Chatterjee SC. 2007. Transgenic Indian mustard (Brassica juncea) expressing tomato glucanase leads to arrested growth of Alternaria brassicae. Plant Cell Rep. 26:247–252.

    • Search Google Scholar
    • Export Citation
  • Moravčíková J, Matušíková I, Libantova J, Bauer M, Mlynárová LU. 2004. Expression of a cucumber class III chitinase and Nicotiana plumbaginifolia class I glucanase genes in transgenic potato plants. Plant Cell Tiss Org Cult (PCTOC). 79:161–8.

    • Search Google Scholar
    • Export Citation
  • Munis MFH, Tu L, Deng F, Tan J, Xu L, Xu S, Long L, Zhang X. 2010. A thaumatin-like protein gene involved in cotton fiber secondary cell wall development enhances resistance against Verticillium dahliae and other stresses in transgenic tobacco. Biochem Biophy Res Communic. 393:38–44.

    • Search Google Scholar
    • Export Citation
  • Muramoto N, Tanaka T, Shimamura T, Mitsukawa N, Hori E, Koda K, Otani M, Hirai M, Nakamura K, Imaeda T. 2012. Transgenic sweet potato expressing thionin from barley gives resistance to black rot disease caused by Ceratocystis fimbriata in leaves and storage roots. Plant Cell Rep. 31:987–997.

    • Search Google Scholar
    • Export Citation
  • Narasimhan ML, Coca MA, Jin J, Yamauchi T, Ito Y, Kadowaki T, Kim KK, Pardo JM, Damsz B, Hasegawa PM, Yun DJ. 2005. Osmotin is a homolog of mammalian adiponectin and controls apoptosis in yeast through a homolog of mammalian adiponectin receptor. Mol Cell. 17:171–180.

    • Search Google Scholar
    • Export Citation
  • Neuhaus JM. 1999. Plant chitinases (PR-3, PR-4, PR-8, PR-11). In: Datta SK, Muthukrishnan S, editors. Pathogenesis-related proteins in plants. Boca Raton, FL: CRC Press; p. 77–105.

    • Search Google Scholar
    • Export Citation
  • Nishizawa Y, Nishio Z, Nakazono K, Soma M, Nakajima E, Ugaki M, Hibi T. 1999. Enhanced resistance to blast (Magnaporthe grisea) in transgenic rice by constitutive expression of rice chitinase. Theor Appl Genet. 99:383–90.

    • Search Google Scholar
    • Export Citation
  • Ntui VO, Thirukkumaran G, Azadi P, Khan RS, Nakamura I, Mii M. 2010. Stable integration and expression of wasabi defensin gene in “Egusi” melon (Colocynthis citrullus L.) confers resistance to Fusarium wilt and Alternaria leaf spot. Plant Cell Rep. 29:943–954.

    • Search Google Scholar
    • Export Citation
  • Okushima Y, Koizumi N, Kusano T, Sano H. 2000. Secreted proteins of tobacco cultured BY2 cells: identification of a new member of pathogenesis-related proteins. Plant Mol Biol. 42(3):479–488.

    • Search Google Scholar
    • Export Citation
  • Oldroyd GE, Staskawicz BJ. 1998. Genetically engineered broad-spectrum disease resistance in tomato. Proc Nat Acad Sci. 95:10300–10305.

    • Search Google Scholar
    • Export Citation
  • Ouyang B, Chen YH, Li HX, Qian CJ, Huang SL, Ye ZB. 2005. Transformation of tomatoes with osmotin and chitinase genes and their resistance to Fusarium wilt. J Hort Sci Biotechnol. 80:517–522.

    • Search Google Scholar
    • Export Citation
  • Ozaki Y, Wada K, Hase T, Matsubara H, Nakanishi T, Yoshizumi H. 1980. Amino acid sequence of a purothionin homolog from barley flour. J Biochem. 87:549–555.

    • Search Google Scholar
    • Export Citation
  • Park CJ, Kim KJ, Shin R, Park JM, Shin YC, Paek KH. 2004. Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway. Plant J. 37:186–198.

    • Search Google Scholar
    • Export Citation
  • Partridge-Telenko DE, Hu J, Livingstone DM, Shew BB, Phipps PM, Grabau EA. 2011. Sclerotinia blight resistance in Virginia-type peanut transformed with a barley oxalate oxidase gene. Phytopathology. 101:786–793.

    • Search Google Scholar
    • Export Citation
  • Patkar RN, Chattoo BB. 2006. Transgenic indica rice expressing ns-LTP-like protein shows enhanced resistance to both fungal and bacterial pathogens. Mol Breed. 17:159–171.

    • Search Google Scholar
    • Export Citation
  • Punja ZK. 2001. Genetic engineering of plants to enhance resistance to fungal pathogens – a review of progress and future prospects. Canad J Plant Pathol. 23:216–235.

    • Search Google Scholar
    • Export Citation
  • Punja ZK. 2004. Genetic engineering of plants to enhance resistance to fungal pathogens. In: Punja ZK, editor. Fungal disease resistance in plants. New York: Food Products Press; p. 207–258.

    • Search Google Scholar
    • Export Citation
  • Punja ZK, Zhang YY. 1993. Plant chitinases and their roles in resistance to fungal diseases. J Nematol. 25:526.

  • Radhajeyalakshmi R, Velazhahan R, Balasubramanian P, Doraiswamy S. 2005. Overexpression of thaumatin-like protein in transgenic tomato plants confers enhanced resistance to Alternaria solani. Arch Phytopathol Plant Prot. 38:257–265.

    • Search Google Scholar
    • Export Citation
  • Rajam MV, Chandola N, Goud PS, Singh D, Kashyap V, Choudhary ML, Sihachakr D. 2007. Thaumatin gene confers resistance to fungal pathogens as well as tolerance to abiotic stresses in transgenic tobacco plants. Biol Plantarum. 51:135–141.

    • Search Google Scholar
    • Export Citation
  • Roy-Barman S, Sautter C, Chattoo BB. 2006. Expression of the lipid transfer protein Ace-AMP1 in transgenic wheat enhances antifungal activity and defense responses. Trans Res. 15:435–446.

    • Search Google Scholar
    • Export Citation
  • Sabater-Jara AB, Almagro L, Belchí-Navarro S, Barceló AR, Pedreño MA. 2011. Methyl jasmonate induces extracellular pathogenesis-related proteins in cell cultures of Capsicum chinense. Plant Sig Behav. 6:440–442.

    • Search Google Scholar
    • Export Citation
  • Schaefer SC, Gasic K, Cammue B, Broekaert W, van Damme EJ, Peumans WJ, Korban SS. 2005. Enhanced resistance to early blight in transgenic tomato lines expressing heterologous plant defense genes. Planta. 222:858–866.

    • Search Google Scholar
    • Export Citation
  • Schestibratov KA, Dolgov SV. 2005. Transgenic strawberry plants expressing a thaumatin II gene demonstrate enhanced resistance to Botrytis cinerea. Sci Horti. 106:177–189.

    • Search Google Scholar
    • Export Citation
  • Schneider M, Droz E, Malno P, Chatot C, Bonnel E, Métraux JP. 2002. Transgenic potato plants expressing oxalate oxidase have increased resistance to oomycete and bacterial pathogens. Pot Res. 45:177–185.

    • Search Google Scholar
    • Export Citation
  • Sels J, Mathys J, De Coninck BM, Cammue BP, De Bolle MF. 2008. Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiol Biochem. 46:941–950.

    • Search Google Scholar
    • Export Citation
  • Shatters RG, Jr, Boykin LM, Lapointe SL, Hunter WB, Weathersbee AA. 2006. Phylogenetic and structural relationships of the PR5 gene family reveal an ancient multigene family conserved in plants and select animal taxa. J Mol Evol. 63:12–29.

    • Search Google Scholar
    • Export Citation
  • Shin S, Mackintosh CA, Lewis J, Heinen SJ, Radmer L, Dill-Macky R, Baldridge GD, Zeyen RJ, Muehlbauer GJ. 2008. Transgenic wheat expressing a barley class II chitinase gene has enhanced resistance against Fusarium graminearum. J Exp Bot. 59:2371–2378.

    • Search Google Scholar
    • Export Citation
  • Simmons CR. 1994. The physiology and molecular biology of plant 1,3-β-D-glucanases and 1,3;1,4-β-D-glucanases. Crit Rev Plant Sci. 13:325–387.

    • Search Google Scholar
    • Export Citation
  • Singh NK, Kumar KRR, Kumar D, Shukla P, Kirti PB. 2013. Characterization of a pathogen induced thaumatin-like protein gene AdTLP from Arachis diogoi, a wild peanut. PLoS One. 8:e83963.

    • Search Google Scholar
    • Export Citation
  • Singh D, Haicour R, Sihachakr D, Rajam MV. 2015. Expression of rice chitinase gene in transgenic eggplant confers resistance to fungal wilts. Ind J Biotechnol. 14:233–240.

    • Search Google Scholar
    • Export Citation
  • Somssich IE, Schmelzer E, Bollmann J, Hahlbrock K. 1986. Rapid activation by fungal elicitor of genes encoding ‘‘pathogenesis-related’’ proteins in cultured parsley cells. Proc Natl Acad Sci USA. 83:2427–2430.

    • Search Google Scholar
    • Export Citation
  • Sridevi G, Parameswari C, Sabapathi N, Raghupathy V, Veluthambi K. 2008. Combined expression of chitinase and β-1, 3-glucanase genes in indica rice (Oryza sativa L.) enhances resistance against Rhizoctonia solani. Plant Sci. 175:283–90.

    • Search Google Scholar
    • Export Citation
  • Stec B. 2006. Plant thionins – the structural perspective. Cell Mol Life Sci CMLS. 63:1370–1385.

  • Sundaresha S, Kumar AM, Rohini S, Math SA, Keshamma E, Chandrashekar SC, Udayakumar M. 2010. Enhanced protection against two major fungal pathogens of groundnut, Cercospora arachidicola and Aspergillus flavus in transgenic groundnut over-expressing a tobacco β 1–3 glucanase. Eur J Plant Pathol. 126:497–508.

    • Search Google Scholar
    • Export Citation
  • Szwacka M, Krzymowska M, Osuch A, Kowalczyk ME, Malepszy S. 2002. Variable properties of transgenic cucumber plants containing the thaumatin II gene from Thaumatococcus daniellii. Act Physiol Planta. 24:173–185.

    • Search Google Scholar
    • Export Citation
  • Takahashi W, Fujimori M, Miura Y, Komatsu T, Nishizawa Y, Hibi T, Takamizo T. 2005. Increased resistance to crown rust disease in transgenic Italian ryegrass (Lolium multiflorum Lam.) expressing the rice chitinase gene. Plant Cell Rep. 23:811–8.

    • Search Google Scholar
    • Export Citation
  • Terras FR, Eggermont K, Kovaleva V, Raikhel NV, Osborn RW, Kester A, Rees SB, Vanderleyden J, Cammue BP, Broekaert WF. 1995. Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell. 7:573–588.

    • Search Google Scholar
    • Export Citation
  • Thevissen K, Kristensen HH, Thomma BPHJ, Cammue BPA, Francois IEJA. 2007. Therapeutic potential of antifungal plant and insects defensins. Drug Discov Today. 12:966–971.

    • Search Google Scholar
    • Export Citation
  • Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J. 2003. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature. 423:74–77.

    • Search Google Scholar
    • Export Citation
  • Tobias DJ, Manoharan M, Pritsch C, Dahleen LS. 2007. Co-bombardment, integration and expression of rice chitinase and thaumatin-like protein genes in barley (Hordeum vulgare cv. Conlon). Plant Cell Rep. 26:631–639.

    • Search Google Scholar
    • Export Citation
  • Vellicce GR, Ricci JC, Hernández L, Castagnaro AP. 2006. Enhanced resistance to Botrytis cinerea mediated by the transgenic expression of the chitinase gene ch5B in strawberry. Trans Res. 15:57–68.

    • Search Google Scholar
    • Export Citation
  • van der Wel, H, Loeve K. 1972. Isolation and characterization of thaumatin I and II, the sweet-tasting proteins from Thaumatococcus daniellii Benth. Eur J Biochem. 31:221–225.

    • Search Google Scholar
    • Export Citation
  • van Loon LC, van Kammen A. 1970. Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var.‘Samsum’ and ‘Samsum NN’. Changes in protein constitution after infection with TMV. Virology. 40:199–211.

    • Search Google Scholar
    • Export Citation
  • van Loon LC. 1982. Regulation of changes in proteins and enzymes associated with active defense against virus infection. In: Wood RKS, editor. Active defense mechanisms in plants. New York: Plenum Press; p. 247–273.

    • Search Google Scholar
    • Export Citation
  • van Loon LC, Pierpont WS, Boller T, Conejero, V. 1994. Recommendations for naming plant pathogenesis-related proteins. Plant Mol Biol Rep. 12:245–264.

    • Search Google Scholar
    • Export Citation
  • van Loon LC, van Strien EA. 1999. The families of pathogenesis- related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol. 55:85–97.

    • Search Google Scholar
    • Export Citation
  • van Loon LC, Rep M, Pieterse CM. 2006. Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol. 44:135–162.

    • Search Google Scholar
    • Export Citation
  • Velazhahan R, Muthukrishnan S. 2003. Transgenic tobacco plants constitutively overexpressing a rice thaumatin-like protein (PR-5) show enhanced resistance to Alternaria alternata. Biol Plantar. 47:347–354.

    • Search Google Scholar
    • Export Citation
  • Vera P, Conejero V. 1988. Pathogenesis-related proteins of tomato P-69 as an alkaline endoproteinase. Plant Physiol. 87:58–63.

  • Wally O, Punja ZK. 2010. Genetic engineering for increasing fungal and bacterial disease resistance in crop plants. GM Crops. 1:199–206.

    • Search Google Scholar
    • Export Citation
  • Wally O, Jayaraj J, Punja Z. 2009. Comparative resistance to foliar fungal pathogens in transgenic carrot plants expressing genes encoding for chitinase, β-1, 3-glucanase and peroxidise. Eur J Plant Pathol. 123:31–42.

    • Search Google Scholar
    • Export Citation
  • Walz A, Zingen‐Sell I, Loeffler M, Sauer M. 2008. Expression of an oxalate oxidase gene in tomato and severity of disease caused by Botrytis cinerea and Sclerotinia sclerotiorum. Plant Pathol. 57:453–458.

    • Search Google Scholar
    • Export Citation
  • Wang Q, Li F, Zhang X, Zhang Y, Hou Y, Zhang S, Wu Z. 2011. Purification and characterization of a CkTLP protein from Cynanchum komarovii seeds that confers antifungal activity. PLoS One. 6:e16930.

    • Search Google Scholar
    • Export Citation
  • Wei YD, Zhang ZG, Andersen CH, Schmelzer E, Gregersen PL, Collinge DB, Smedegaard-Petersen V, Thordal-Christensen H. 1998. An epidermis/papilla-specific oxidase-like protein in the defence response of barley attacked by the powdery mildew fungus. Plant Mol Biol. 36:101–112.

    • Search Google Scholar
    • Export Citation
  • Woloshuk CP, Meulenhoff JS, Sela-Buurlage M, Van den Elzen PJM, Cornelissen BJC. 1991. Pathogen-induced proteins with inhibitory activity toward Phytophthora infestans. Plant Cell. 3:619–628.

    • Search Google Scholar
    • Export Citation
  • Wróbel-Kwiatkowska M, Lorenc-Kukula K, Starzycki M, Oszmiański J, Kepczyńska E, Szopa J. 2004. Expression of β-1,3-glucanase in flax causes increased resistance to fungi. Physiol Mol Plant Pathol. 65:245–256.

    • Search Google Scholar
    • Export Citation
  • Xiao YH, Li XB, Yang XY, Luo M, Hou L, Guo SH, Luo XY, Pei Y. 2007. Cloning and characterization of a balsam pear class I chitinase gene (Mcchit1) and its ectopic expression enhances fungal resistance in transgenic plants. Biosci Biotechnol Biochem. 71:1211–1219.

    • Search Google Scholar
    • Export Citation
  • Xie YR, Chen ZY, Brown RL, Bhatnagar D. 2010. Expression and functional characterization of two pathogenesis-related protein 10 genes from Zea mays. J Plant Physiol. 67:121–130.

    • Search Google Scholar
    • Export Citation
  • Xu P, Jiang L, Wu J, Li W, Fan S, Zhang S. 2014. Isolation and characterization of a pathogenesis-related protein 10 gene (GmPR10) with induced expression in soybean (Glycine max) during infection with Phytophthora sojae. Mol Biol Rep. 41:4899–4909.

    • Search Google Scholar
    • Export Citation
  • Xue X, Cao ZX, Zhang XT, Wang Y, Zhang YF, Chen ZX, Pan XB, Zuo SM. 2016. Overexpression of OsOSM1 enhances resistance to rice sheath blight. Plant Dis. 100:1634–1642.

    • Search Google Scholar
    • Export Citation
  • Yadav S, Srivastava AK, Singh DP, Arora DK. 2012. Isolation of oxalic acid tolerating fungi and decipherization of its potential to control Sclerotinia sclerotiorum through oxalate oxidase like protein. World J Microbiol Biotechnol. 28:3197–3206.

    • Search Google Scholar
    • Export Citation
  • Yamamoto T, Iketani H, Ieki H, Nishizawa Y, Notsuka K, Hibi T, Hayashi T, Matsuta N. 2000. Transgenic grapevine plants expressing a rice chitinase with enhanced resistance to fungal pathogens. Plant Cell Rep. 19:639–646.

    • Search Google Scholar
    • Export Citation
  • Yang CY, Hoa YC, Panga JC, Huang SS, Tschen JSM. 2009. Cloning and expression of an antifungal chitinase gene of a novel Bacillus subtilis isolate from Taiwan potato field. Biores Technol. 100:1454–1458.

    • Search Google Scholar
    • Export Citation
  • Yun DJ, Ibeas JI, Lee H, Coca MA, Narasimhan ML, Uesono Y, Hasegawa PM, Pardo JM, Bressan RA. 1998. Osmotin, a plant antifungal protein, subverts signal transduction to enhance fungal cell susceptibility. Mol Cell. 1:807–817.

    • Search Google Scholar
    • Export Citation
  • Zasloff M. 2002. Antimicrobial peptides of multicellular organisms. Nature. 415:389–395.

  • Zhang Z, Collinge DB, Thordal-Christensen H. 1995. Germin-like oxalate oxidase, a H2O2-producing enzyme, accumulates in barley attacked by the powdery mildew fungus. Plant J. 8:139–145.

    • Search Google Scholar
    • Export Citation
  • Zhu BL, Chen THH, Li PH. 1995. Expression of three osmotin-like protein genes in response to osmotic stress and fungal infection in potato. Plant Mol Biol. 28:17–26.

    • Search Google Scholar
    • Export Citation

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