Plant Cell Reports

, Volume 29, Issue 5, pp 419–436 | Cite as

The superfamily of thaumatin-like proteins: its origin, evolution, and expression towards biological function

  • Jun-Jun LiuEmail author
  • Rona Sturrock
  • Abul K. M. Ekramoddoullah


Thaumatin-like proteins (TLPs) are the products of a large, highly complex gene family involved in host defence and a wide range of developmental processes in fungi, plants, and animals. Despite their dramatic diversification in organisms, TLPs appear to have originated in early eukaryotes and share a well-defined TLP domain. Nonetheless, determination of the roles of individual members of the TLP superfamily remains largely undone. This review summarizes recent advances made in elucidating the varied TLP activities related to host resistance to pathogens and other physiological processes. Also discussed is the current state of knowledge on the origins and types of TLPs, regulation of gene expression, and potential biotechnological applications for TLPs.


Antifungal activity Defence response Environmental stress Phylogenetic analysis Thaumatin-like protein 



Anti-freeze protein


G protein-coupled receptors


Million years ago


Osmotin-like protein




Family 5 of pathogenesis-related proteins


PR5-like kinase


Thaumatin-like protein



This work is supported in part by the Canadian Forest Service and the CFS-Genome R&D Initiative.


  1. Abad LR, D’Urzo MP, Liu D, Narasimhan ML, Reuveni M, Zhu JK, Niu X, Singh NK, Hasegawa PM, Bressen RA (1996) Antifungal activity of tobacco osmotin has specificity and involves plasma membrane permeabilization. Plant Sci 118:11–23CrossRefGoogle Scholar
  2. 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 54:1101–1111PubMedCrossRefGoogle Scholar
  3. Anžlovar S, Dermastia M (2003) The comparative analysis of osmotins and osmotin-like PR-5 proteins. Plant Biol 5:116–124CrossRefGoogle Scholar
  4. Barre A, Peumans WJ, Menu-Bouaouiche L, Van Damme EJM, May GD, Herrera AF, Van Leuven F, Rougé P (2000) Purification and structural analysis of an abundant thaumatin-like protein from ripe banana fruit. Planta 211:791–799PubMedCrossRefGoogle Scholar
  5. Barthakur S, Babu V, Bansal KC (2001) Overexpression of osmotin induces proline accumulation and confers tolerance to osmotic stress in transgenic tobacco. J Plant Biochem Biotechnol 10:31–37Google Scholar
  6. Bartoszewski G, Niedziela A, Szwacka M, Niemirowicz-Szczytt K (2003) Modification of tomato taste in transgenic plants carrying a thaumatin gene from Thaumatococcus daniellii Benth. Plant Breed 122:347–351CrossRefGoogle Scholar
  7. Batalia MA, Monzingo AF, Ernst S, Roberts W, Robertus JD (1996) The crystal structure of the antifungal protein zeamatin, a member of the thaumatin-like, PR-5 protein family. Nat Struct Biol 3:19–23PubMedCrossRefGoogle Scholar
  8. Bormann C, Baier D, Hörr I, Raps C, Berger J, Jung G, Schwarz H (1999) Characterization of a novel, antifungal, chitin-binding protein from Streptomyces tendae Tü901 that interferes with growth polarity. J Bacteriol 181:7421–7429PubMedGoogle Scholar
  9. Brandazza A, Angeli S, Tegoni M, Cambillau C, Pelosi P (2004) Plant stress proteins of the thaumatin-like family discovered in animals. FEBS Lett 572:3–7PubMedCrossRefGoogle Scholar
  10. Breiteneder H (2004) Thaumatin-like proteins—a new family of pollen and fruit allergens. Allergy 59:479–481PubMedCrossRefGoogle Scholar
  11. Brito N, Espino JJ, Gonzalez C (2006) The endo-β-1, 4-xylanase Xyn11A is required for virulence in Botrytis cinerea. Mol Plant Microbe Interact 19:25–32PubMedCrossRefGoogle Scholar
  12. Campos MA, Silva MS, Magalhães CP, Ribeiro SG, Sarto RPD, Vieira EA, Grossi de Sá MF (2008) Expression in Escherichia coli, purification, refolding and antifungal activity of an osmotin from Solanum nigrum. Microbial Cell Factories 7:7CrossRefGoogle Scholar
  13. Christensen AB, Cho BH, Naesby M, Gregersen PL, Brandt J, Madri-Ordenãna K, Collinge DB, Thordal-Christensen H (2002) The molecular characterization of two barley proteins establishes the novel PR-17 family of pathogenesis-related proteins. Mol Plant Pathol 3:135–144PubMedCrossRefGoogle Scholar
  14. Chu KT, Ng TB (2003) Isolation of a large thaumatin-like antifungal protein from seeds of the Kweilin chestnut Castanopsis chinensis. Biochem Biophys Res Commun 301:364–370PubMedCrossRefGoogle Scholar
  15. Coca MA, Damsz B, Yun D-J, Hasegawa PM, Bressan RA, Narasimhan ML (2000) Heterotrimeric G proteins of a filamentous fungus regulate cell wall composition and susceptibility to a plant PR-5 protein. Plant J 22:61–69PubMedCrossRefGoogle Scholar
  16. Cortegano I, Civantos E, Aceituno E, del Moral A, Lopez E, Lombardero M, del Pozo V, Lahoz C (2004) Cloning and expression of a major allergen from Cupressus arizonica pollen, Cup a 3, a PR-5 protein expressed under polluted environment. Allergy 59:485–490PubMedCrossRefGoogle Scholar
  17. D’Angeli S, Altamura MM (2007) Osmotin induces cold protection in olive trees by affecting programmed cell death and cytoskeleton organization. Planta 225:1147–1163PubMedCrossRefGoogle Scholar
  18. Dall’Antonia Y, Pavkov T, Fuchs H, Breiteneder H, Kellera W (2005) Crystallization and preliminary structure determination of the plant food allergen Pru av 2. Acta Crystallogr Sect F Struct Biol Cryst Commun 61(Pt2):186–188PubMedCrossRefGoogle Scholar
  19. Datta K, Velazhahan R, Oliva N, Ona I, Mew T, Kush 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 98:1138–1145CrossRefGoogle Scholar
  20. Doolittle RF, Feng DF, Tsang S, Cho G, Little E, Storrs UCT (1996) Determining divergence times of the major kingdoms of living organisms with a protein clock. Science 271(5248):470–477PubMedCrossRefGoogle Scholar
  21. Doxey AC, Yaish MW, Griffith M, McConkey BJ (2006) Ordered surface carbons distinguish antifreeze proteins and their ice-binding regions. Nat Biotechnol 24:852–855PubMedCrossRefGoogle Scholar
  22. 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 Breeding 7:175–185CrossRefGoogle Scholar
  23. Faus I (2000) Recent developments in the characterization and biotechnological production of sweet-tasting proteins. Appl Microbial Biotechnol 53:145–151CrossRefGoogle Scholar
  24. 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 403:583–591PubMedCrossRefGoogle Scholar
  25. Fierens E, Gebruers K, Voet AR, De Maeyer M, Courtin CM, Delcour JA (2009) Biochemical and structural characterization of TLXI, the Triticum aestivum L. thaumatin-like xylanase inhibitor. J Enzyme Inhib Med Chem 24:646–654PubMedCrossRefGoogle Scholar
  26. Franco OL, Rigden DJ, Melo FR, Grossi-De-Sá MF (2002) Plant alpha-amylase inhibitors and their interaction with insect alpha-amylases. Eur J Biochem 269:397–412PubMedCrossRefGoogle Scholar
  27. 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 168:671–680CrossRefGoogle Scholar
  28. Fuchs HC, Hoffmann-Sommergruber K, Wagner B, Krebitz M, Scheiner O, Breiteneder H (2002) Heterologous expression in Nicotiana benthamiana of Cap a 1, a thaumatin-like protein and major allergen from bell pepper (Capsicum annuum). J Allergy Clin Immunol 109:S134CrossRefGoogle Scholar
  29. Fujimura T, Futamura N, Midoro-Horiuti T, Togawa A, Goldblum RM, Yasueda H, Saito A, Shinohara K, Masuda K, Kurata K, Sakaguchi M (2007) Isolation and characterization of native Cry j 3 from Japanese cedar (Cryptomeria japonica) pollen. Allergy 62:547–553PubMedCrossRefGoogle Scholar
  30. Futamura N, Tani N, Tsumura Y, Nakajima N, Sakaguchi M, Shinohara K (2006) Characterization of genes for novel thaumatin-like proteins in Cryptomeria japonica. Tree Physiol 26:51–62PubMedCrossRefGoogle Scholar
  31. Gao ZS, Weg WE, Schaart JG, Arkel G, Breiteneder H, Hoffmann-Sommergruber K, Gilissen LJ (2005) Genomic characterization and linkage mapping of the apple allergen genes Mal d 2 (thaumatin-like protein) and Mal d 4 (profilin). Theor Appl Genet 111:1087–1097PubMedCrossRefGoogle Scholar
  32. Garcia-casado G, Collada C, Allona I, Soto A, Casado R, Rodriguez-cerezo E, Gomez L, Aragoncillo C (2000) Characterization of an apoplastic basic thaumatin-like protein from recalcitrant chestnut seeds. Physiol Plant 110:172–180CrossRefGoogle Scholar
  33. Gavrović-Jankulović M, Ćirković T, Vučković O, Atanasković-Marković M, Petersen A, Gojgić G, Burazer L, Jankov RM (2002) Isolation and biochemical characterization of a thaumatin-like kiwi allergen. J Allergy Clin Immunol 110:805–810PubMedCrossRefGoogle Scholar
  34. Ghosh R, Chakrabarti C (2008) Crystal structure analysis of NP24-I: a thaumatin-like protein. Planta 228:883–890PubMedCrossRefGoogle Scholar
  35. Gómez-Leyvaa JF, Blanco-Labraa A (2001) Bifunctional α-amylase/trypsin inhibitor activity previously ascribed to the 22 KDa TL protein, resided in a contaminant protein of 14 KDa. J Plant Physiol 158:177–183CrossRefGoogle Scholar
  36. Greenstein S, Shadkchan Y, Jadoun J, Sharon C, Markovich S, Osherov N (2006) Analysis of the Aspergillus nidulans thaumatin-like cetA gene and evidence for transcriptional repression of pyr4 expression in the cetA-disrupted strain. Fungal Genet Biol 43:42–53PubMedCrossRefGoogle Scholar
  37. Grenier J, Potvin C, Trudel J, Asselin A (1999) Some thaumatin-like proteins hydrolyse polymeric β-1, 3-glucans. Plant J 19:473–480PubMedCrossRefGoogle Scholar
  38. Grenier J, Potvin C, Asselin A (2000) Some fungi express β-1, 3-glucanases similar to thaumatin-like proteins. Mycologia 92:841–848CrossRefGoogle Scholar
  39. Griffith M, Yaish MWF (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9:399–405PubMedCrossRefGoogle Scholar
  40. Griffith M, Lumb C, Wiseman SB, Wisniewski M, Johnson RW, Marangoni AG (2005) Antifreeze proteins modify the freezing process in planta. Plant Physiol 138:330–340PubMedCrossRefGoogle Scholar
  41. Guo Z, Bonos S, Meyer WA, Day PR, Belanger FC (2003) Transgenic creeping bentgrass with delayed dollar spot symptoms. Mol Breeding 11:95–101CrossRefGoogle Scholar
  42. Hiroyuki K, Terauchi R (2008) Regulation of expression of rice thaumatin-like protein: inducibility by elicitor requires promoter W-box elements. Plant Cell Rep 27:1521–1528PubMedCrossRefGoogle Scholar
  43. Ho VS, Wong JH, Ng TB (2007) A thaumatin-like antifungal protein from the emperor banana. Peptides 28:760–766PubMedCrossRefGoogle Scholar
  44. Hoffmann-Sommergruber K (2002) Pathogenesis-related (PR)-proteins identified as allergens. Biochem Soc Trans 30:930–935PubMedCrossRefGoogle Scholar
  45. Hulo N, Bairoch A, Bulliard V, Cerutti L, Cuche BA, de Castro E, Lachaize C, Langendijk-Genevaux PS, Sigrist CJ (2008) The 20 years of PROSITE. Nucleic Acids Res 36(database issue):D245–249Google Scholar
  46. Husaini AM, Abdin MZ (2008) Development of transgenic strawberry (Fragaria x ananassa Dutch.) plants tolerant to salt stress. Plant Sci 174:446–455CrossRefGoogle Scholar
  47. Ibeas JI, Lee H, Damsz B, Prasad DT, Pardo JM, Hasegawa PM, Bressan RA, Narasimhan ML (2000) Fungal cell wall phosphomannans facilitate the toxic activity of a plant PR-5 protein. Plant J 23:375–383PubMedCrossRefGoogle Scholar
  48. Ibeas JI, Yun D-J, Damsz B, Narasimhan ML, Uesono Y, Ribas JC, Lee H, Hasegawa PM, Bressan RA, Pardo JM (2001) Resistance to the plant PR-5 protein osmotin in the model fungus Saccharomyces cerevisiae is mediated by the regulatory effects of SSD1 on cell wall composition. Plant J 25:271–280PubMedCrossRefGoogle Scholar
  49. Inschlag C, Hoffmann-Sommergruber K, O’Riordain G, Ahorn H, Ebner C, Scheiner O, Breiteneder H (1998) Biochemical characterization of Pru a 2, a 23-kD thaumatin-like protein representing a potential major allergen in cherry (Prunus avium). Int Arch Allergy Immunol 116:22–28PubMedCrossRefGoogle Scholar
  50. Jami SK, Swathi Anuradha T, Guruprasad L, Kirti PB (2007) Molecular, biochemical and structural characterization of osmotin-like protein from black nightshade (Solanum nigrum). J Plant Physiol 164:238–252PubMedCrossRefGoogle Scholar
  51. Jayasankar S, Li Z, Gray DJ (2003) Constitutive expression of Vitis vinifera thaumatin-like protein after in vitro selection and its role in anthracnose resistance. Funct Plant Biol 30:1105–1115CrossRefGoogle Scholar
  52. Jung YC, Lee HJ, Yum SS, Soh WY, Cho DY, Auh CK, Lee TK, Soh HC, Kim YS, Lee SC (2005) Drought-inducible-but ABA-independent-thaumatin-like protein from carrot (Daucus carota L.). Plant Cell Rep 24:366–373PubMedCrossRefGoogle Scholar
  53. Kalpana K, Maruthasalama S, Rajesha T, Poovannana K, Kumara KK, Kokiladevia E, Rajaa JAJ, Sudhakara D, Velazhahanb R, Samiyappanb R, Balasubramaniana P (2006) Engineering sheath blight resistance in elite indica rice cultivars using genes encoding defense proteins. Plant Sci 170:203–215CrossRefGoogle Scholar
  54. Kaneko R, Kitabatake N (2001) Structure-sweetness relationship in thaumatin: importance of lysine residues. Chem Senses 26:167–177PubMedCrossRefGoogle Scholar
  55. Kenton P, Darby RM, Shelley G, Draper J (2000) A PR-5 gene promoter from Asparagus officinalis (AoPRT-L) is not induced by abiotic stress, but is activated around sites of pathogen challenge and by salicylate in transgenic tobacco. Mol Plant Pathol 1:367–378PubMedCrossRefGoogle Scholar
  56. Kim YS, Park JY, Kim KS, Ko MK, Cheong SJ, Oh BJ (2002) A thaumatin-like gene in nonclimacteric pepper fruits used as molecular marker in probing disease resistance, ripening, and sugar accumulation. Plant Mol Biol 49:125–135PubMedCrossRefGoogle Scholar
  57. Kim MJ, Ham BK, Kim HR, Lee IJ, Kim YJ, Ryu KH, Park YI, Paek KH (2005) In vitro and in planta interaction evidence between Nicotiana tabacum thaumatin-Like protein 1 (TLP1) and cucumber mosaic virus proteins. Plant Mol Biol 59:981–994PubMedCrossRefGoogle Scholar
  58. Kitajima S, Sato F (1999) Plant pathogenesis-related proteins: molecular mechanisms of gene expression and protein function. J Biochem (Tokyo) 125:1–8Google Scholar
  59. Kobayashi K, Fukuda M, Igarashi D, Sunaoshi M (2000) Cytokinin-binding proteins from tobacco callus share homology with osmotin-like protein and an nndochitinase. Plant Cell Physiol 41:148–157PubMedGoogle Scholar
  60. Koiwa H, Kato H, Nakatsu T, Oda J, Yamada Y, Sato F (1999) Crystal structure of tobacco PR-5d protein at 1.8Å resolution reveals a conserved acidic cleft structure in antifungal thaumatin-like proteins. J Mol Biol 286:1137–1145PubMedCrossRefGoogle Scholar
  61. 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 D2, a thaumatin-like protein and allergen of apple (Malus domestica), and its characterization as an antifungal protein. J Mol Biol 329:721–730PubMedCrossRefGoogle Scholar
  62. Kuwabara C, Takezawa D, Shimada T, Hamada T, Fujikawa S, Arakawa K (2002) Abscisic acid- and cold-induced thaumatin-like protein in winter wheat has antifungal activity against snow mould, Microdochium nivale. Physiol Plant 115:101–110PubMedCrossRefGoogle Scholar
  63. Leone P, Menu-Bouaouiche L, Peumans WJ, Payan F, Barre A, Roussel A, Van Damme EJ, Rougé P (2006) Resolution of the structure of the allergenic and antifungal banana fruit thaumatin-like protein at 1.7-A. Biochimie 88:45–52PubMedCrossRefGoogle Scholar
  64. Léon-Kloosterziel KM, Verhagen BW, Keurentjes JJ, VanPelt JA, Rep M, VanLoon LC, Pieterse CM (2005) Colonization of the Arabidopsis rhizosphere by fluorescent Pseudomonas spp. activates a root-specific, ethylene-responsive PR-5 gene in the vascular bundle. Plant Mol Biol 57:731–748PubMedCrossRefGoogle Scholar
  65. Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E (2002) Human receptors for sweet and umami taste. Proc Natl Acad Sci USA 99:4692–4696PubMedCrossRefGoogle Scholar
  66. Liu J-J, Zamani A, Ekramoddoullah AKM (2010) Expression profiling of a complex thaumatin-like protein family in western white pine. Planta 231:637–651PubMedCrossRefGoogle Scholar
  67. Lorito M, Woo SL, D’Ambrosio M, Harman GE, Hayes CK, Kubicek CP, Scala F (1996) Synergistic interaction between cell wall degrading enzymes and membrane affecting compounds. Mol Plant-Microbe Interact 9:206–213CrossRefGoogle Scholar
  68. Mackintosh CA, Lewis J, Radmer LE, Shin S, Heinen SJ, Smith LA, Wyckoff MN, Dill-Macky R, Evans CK, Kravchenko S, Baldridge GD, Zeyen RJ, Muehlbauer GJ (2007) Overexpression of defense response genes in transgenic wheat enhances resistance to Fusarium head blight. Plant Cell Rep 26:479–488PubMedCrossRefGoogle Scholar
  69. Maria S, Magdalena K, Anita O, Magdalena K, Stefan M (2002) Variable properties of transgenic cucumber plants containing the thaumatin II gene from Thaumatococcus daniellii. Acta Physiol Plant 24:173–185CrossRefGoogle Scholar
  70. Martin K, McDougall BM, McIlroy S, Jayus ChenJ, Seviour RJ (2007) Biochemistry and molecular biology of exocellular fungal β-(1,3)- and β-(1,6)-glucanases. FEMS Microbiol Rev 31:168–192PubMedCrossRefGoogle Scholar
  71. Maruthasalam S, Kalpana K, Kumar KK, Loganathan M, Poovannan K, Raja JA, Kokiladevi E, Samiyappan R, Sudhakar D, Balasubramanian P (2007) Pyramiding transgenic resistance in elite indica rice cultivars against the sheath blight and bacterial blight. Plant Cell Rep 26:791–804PubMedCrossRefGoogle Scholar
  72. Masudaa T, Kitabatake N (2006) Developments in biotechnological production of sweet proteins. J Biosci Bioeng 102:375–389CrossRefGoogle Scholar
  73. Menu-Bouaouichea L, Vrieta C, Peumansb WJ, Barrea A, Van Dammec EJM, Rougé P (2003) A molecular basis for the endo-β1, 3-glucanase activity of the thaumatin-like proteins from edible fruits. Biochimie 85:123–131CrossRefGoogle Scholar
  74. Middleton AJ, Brown AM, Daviesa PL, Walker VK (2009) Identification of the ice-binding face of a plant antifreeze protein. FEBS Lett 583:815–819PubMedCrossRefGoogle Scholar
  75. Midoro-Horiuti T, Goldblum RM, Kurosky A, Wood TG, Brooks EG (2000) Variable expression of pathogenesis-related protein allergen in mountain cedar (Juniperus ashei) pollen. J Immunol 164:2188–2192PubMedGoogle Scholar
  76. Min K, Ha SC, Hasegawa PM, Bressan RA, Yun D-J, Kim KK (2004) Crystal structure of osmotin, a plant antifungal protein. Proteins Struct Funct Bioinform 54:170–173CrossRefGoogle Scholar
  77. Monteiro S, Barakat M, Piçarra-Pereira MA, Teixeira AR, Ferreira RB (2003) Osmotin and thaumatin from grape: a putative general defense mechanism against pathogenic fungi. Phytopathology 93:1505–1512PubMedCrossRefGoogle Scholar
  78. Narasimhan ML, Damsz B, Coca MA, Ibeas JI, Yun DJ, Pardo JM, Hasegawa PM, Bressan RA (2001) A plant defense response effector induces microbial apoptosis. Mol Cell 8:921–930PubMedCrossRefGoogle Scholar
  79. Narasimhan ML, Lee H, Damsz B, Singh NK, Ibeas JL, Matsumoto TK, Woloshuk CP, Bressan RA (2003) Overexpression of a cell wall glycoprotein in Fusarium oxysporum increases virulence and resistance to a plant PR-5 protein. Plant J 36:390–400PubMedCrossRefGoogle Scholar
  80. Narasimhan M, Coca M, Jin J, Yamauchi T, Ito Y, Kadowaki T, Kim K, Pardo J, Damsz B, Hasegawa P (2005) Osmotin is a homolog of mammalian adiponectin and controls apoptosis in yeast through a homolog of mammalian adiponectin receptor. Mol Cell 17:171–180PubMedCrossRefGoogle Scholar
  81. Newton S, Duman JG (2000) An osmotin-like cryoprotective protein from bittersweet nightshade Solanum dulcamara. Plant Mol Biol 44:581–589PubMedCrossRefGoogle Scholar
  82. O’Leary SJ, Poulis BA, von Aderkas P (2007) Identification of two thaumatin-like proteins (TLPs) in the pollination drop of hybrid yew that may play a role in pathogen defence during pollen collection. Tree Physiol 27:1649–1659PubMedGoogle Scholar
  83. Ogata CM, Gordon PF, de Vos AM, Kim SH (1992) Crystal structure of a sweet tasting protein thaumatin I, at 1.65 A resolution. J Mol Biol 228:893–908PubMedCrossRefGoogle Scholar
  84. Onishi M, Tachi H, Kojima T, Shiraiwa M, Takahara H (2006) Molecular cloning and characterization of a novel salt-inducible gene encoding an acidic isoform of PR-5 protein in soybean (Glycine max [L.] Merr.). Plant Physiol Biochem 44:574–580PubMedCrossRefGoogle Scholar
  85. Osherov N, Mathew J, Romans A, May GS (2002) Identification of conidial-enriched transcripts in Aspergillus nidulans using suppression subtractive hybridization. Fungal Genet Biol 37:197–204PubMedCrossRefGoogle Scholar
  86. Osmond RIW, Hrmova M, Fontaine F, Imberty A, Fincher GB (2001) Binding interactions between barley thaumatin-like proteins and (1, 3)-ß-D-glucans. Eur J Biochem 15:4190–4199CrossRefGoogle Scholar
  87. Parkhi V, Kumar V, Sunilkumar G, Campbell LM, Singh NK, Rathore KS (2009) Expression of apoplastically secreted tobacco osmotin in cotton confers drought tolerance. Mol Breeding 23:625–639CrossRefGoogle Scholar
  88. Pastorello EA, Farioli L, Pravettoni V, Ortolani C, Fortunato D, Giuffrida MG, Perono Garoffo L, Calamari AM, Brenna O, Conti A (2003) Identification of grape and wine allergens as an endochitinase 4, a lipid-transfer protein, and a thaumatin. J Allergy Clin Immunol 111:350–359PubMedCrossRefGoogle Scholar
  89. Perri F, Romitelli F, Rufini F, Secundo F, Stasio ED, Giardina B, Vitali A (2008) Different structural behaviors evidenced in thaumatin-like proteins: a spectroscopic study. Protein J 27:13–20PubMedCrossRefGoogle Scholar
  90. Piggott N, Ekramoddoullah AKM, Liu J-J, Yu X (2004) Gene cloning and expression of a thaumatin-like protein of western white pine (Pinus monticola D.Don). Physiol Mol Plant Pathol 64:1–8CrossRefGoogle Scholar
  91. Raghothama KG, Maggio A, Narasimhan ML, Kononowicz AK (1997) Tissue-specific activation of the osmotin gene by ABA, C2H4 and NaCl involves the same promoter region. Plant Mol Biol 34:393–402PubMedCrossRefGoogle Scholar
  92. 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 Plant 51:135–141CrossRefGoogle Scholar
  93. Regalado AP, Ricardo CPP (1996) Study of intercellular fluid in healthy Lupinus albus organs. Plant Physiol 110:227–232PubMedCrossRefGoogle Scholar
  94. Rep M, Dekker HL, Vossen JH, de Boer AD, Houterman PM, Speijer D, Back JW, de Koster CG, Cornelissen BJC (2002) Mass spectrometric identification of isoforms of PR proteins in xylem sap of fungus-infected tomato. Plant Physiol 130:904–917PubMedCrossRefGoogle Scholar
  95. Richardson M, Valdes-Rodriquez S, Blanco-Labra A (1987) A possible function for thaumatin and a TMV-induced protein suggested by homology to a maize inhibitor. Nature 327:432–434CrossRefGoogle Scholar
  96. Roberts WK, Selitrennikoff CP (1990) Zeamatin, an antifungal protein from maize with membrane-permeabilizing activity. J Gen Microbiol 136:1771–1778Google Scholar
  97. Rombouts S, Fierens E, Vandermarliere E, Voet A, Gebruers K, Beaugrand J, Courtin CM, Delcour JA, de Maeyer M, Rabijns A, Van Campenhout S, Volckaert G (2009) His22 of TLXI plays a critical role in the inhibition of glycoside hydrolase family 11 xylanases. J Enzyme Inhib Med Chem 24:38–46PubMedCrossRefGoogle Scholar
  98. Ruiz CRA, Herrera C, Ghislain M, Gebhardt C (2005) Organization of phenylalanine ammonia lyase (PAL), acidic PR-5 and osmotin-like (OSM) defence-response gene families in the potato genome. Mol Genet Genomics 274:168–179CrossRefGoogle Scholar
  99. Sakamoto Y, Watanabe H, Nagai M, Nakade K, Takahashi M, Sato T (2006) Lentinula edodes tlg1 encodes a thaumatin-like protein that is involved in Lentinan degradation and fruiting body senescence. Plant Physiol 141:793–801PubMedCrossRefGoogle Scholar
  100. Salzman RA, Koiwa H, Ibeas JI, Pardo JM, Hasegawa PM, Bressan RA (2004) Inorganic cations mediate plant PR5 protein antifungal activity through fungal Mnn1- and Mnn4-regulated cell surface glycans. Mol Plant Microbe Interact 17:780–788PubMedCrossRefGoogle Scholar
  101. Sassa H, Ushijima K, Hirano H (2002) A pistil-specific thaumatin/PR5-like protein gene of Japanese pear (Pyrus serotina): sequence and promoter activity of the 5′ region in transgenic tobacco. Plant Mol Biol 50:371–377PubMedCrossRefGoogle Scholar
  102. Schestibratov KA, Dolgov SV (2005) Transgenic strawberry plants expressing a thaumatin II gene demonstrate enhanced resistance to Botrytis cinerea. Sci Hortic 106:177–189CrossRefGoogle Scholar
  103. Schimoler-O’Rourke R, Richardson M, Selitrennikoff CP (2001) Zeamatin inhibits trypsin and α-amylase activities. Appl Environ Microbiol 67:2365–2366PubMedCrossRefGoogle Scholar
  104. Selitrennikoff CP, Wilson SJ, Clemons KV, Stevens DA (2000) Zeamatin, an antifungal protein. Curr Opin Anti-Infective Drugs 2:368–374Google Scholar
  105. Shatters RG Jr, Boykin LM, Lapointe SL, Hunter WB, Weathersbee AA 3rd (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 63:12–29PubMedCrossRefGoogle Scholar
  106. Shiu S-H, Bleecker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98:10763–10768PubMedCrossRefGoogle Scholar
  107. Singh NK, Nelson DE, Kuhn D, Hasegawa PM, Bressan PA (1989) Molecular cloning of osmotin and regulation of its expression by ABA and adaptation to low water potential. Plant Physiol 90:1096–1101PubMedCrossRefGoogle Scholar
  108. Skadsen RW, Sathish P, Kaeppler HF (2000) Expression of thaumatin-like permatin PR-5 genes switches from the ovary wall to the aleurone in developing barley and oat seeds. Plant Sci 156:11–22PubMedCrossRefGoogle Scholar
  109. Smole U, Bublin M, Radauer C, Ebner C, Breiteneder H (2008) Mal d 2, the thaumatin-like allergen from apple, is highly resistant to gastrointestinal digestion and thermal processing. Int Arch Allergy Immunol 147:289–298PubMedCrossRefGoogle Scholar
  110. Tachi H, Fukuda-Yamada K, Kojima T, Shiraiwa M, Takahara H (2009) Molecular characterization of a novel soybean gene encoding a neutral PR-5 protein induced by high-salt stress. Plant physiol biochem 47:73–79PubMedCrossRefGoogle Scholar
  111. Takemoto D, Furuse K, Doke N, Kawakita K (1997) Identification of chitinase and osmotin-like protein as actin-binding proteins in suspension-cultured potato cells. Plant Cell Physiol 38:441–448PubMedGoogle Scholar
  112. Trudel J, Grenier J, Potvin C, Asselin A (1998) Several thaumatin-like proteins bind to 1, 3-glucans. Plant Physiol 118:1431–1438PubMedCrossRefGoogle Scholar
  113. Tsukuda S, Gomi K, Yamamoto H, Akimitsu K (2006) Characterization of cDNAs encoding two distinct miraculin-like proteins and stress-related modulation of the corresponding mRNAs in Citrus jambhiri lush. Plant Mol Biol 60:125–136PubMedCrossRefGoogle Scholar
  114. Van Damme EJ, Charels D, Menu-Bouaouiche L, Proost P, Barre A, Rougé P, Peumans WJ (2002) Biochemical, molecular and structural analysis of multiple thaumatin-like proteins from the elderberry tree (Sambucus nigra L.). Planta 214:853–862PubMedCrossRefGoogle Scholar
  115. Van der Wel H, Loewe K (1972) Isolation and characterization of thaumatin I and II, the sweet-tasting proteins from Thaumatococcus daniellii Benth. Eur J Biochem 31:221–225PubMedCrossRefGoogle Scholar
  116. Van Loon LC, Rep M, Pieterse CM (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162PubMedCrossRefGoogle Scholar
  117. Velazhahan R, Muthukrishnan S (2003) Transgenic tobacco plants constitutively overexpressing a rice thaumatin-like protein (PR-5) show enhanced resistance to Alternaria alternate. Biol Plant 47:347–354CrossRefGoogle Scholar
  118. Velazhahan R, Datta SK, Muthukrishnan S (1999) The PR-5 family: thaumatin-like proteins in plants. In: Datta SK, Muthukrishnan S (eds) Pathogenesis-related proteins in plants. CRC Press, Boca Raton, pp 107–129Google Scholar
  119. Veronese P, Ruiz MT, Coca MA, Hernandez-Lopez A, Lee H, Ibeas JI, Damsz B, Pardo JM, Hasegawa PM, Bressan RA, Narasimhan ML (2003) In defense against pathogens: both plant sentinels and foot soldiers need to know the enemy. Plant Physiol 131:1580–1590PubMedCrossRefGoogle Scholar
  120. Vitali A, Pacini L, Bordi E, De Mori P, Pucillo L, Maras B, Botta B, Brancaccio A, Giardina B (2006) Purification and characterization of an antifungal thaumatin-like protein from Cassia didymobotrya cell culture. Plant Physiol Biochem 44:604–610PubMedCrossRefGoogle Scholar
  121. Wang L, Duman JG (2006) A thaumatin-like protein from larvae of the beetle Dendroides canadensis enhances the activity of antifreeze proteins. Biochem 45:1278–1284CrossRefGoogle Scholar
  122. Wang X, Zafian P, Choudhary M, Lawton M (1996) The PR5 K receptor protein kinase from Arabidopsis thaliana is structurally related to a family of plant defense proteins. Proc Natl Acad Sci USA 93:2598–2602PubMedCrossRefGoogle Scholar
  123. Wellman CH, Osterloff PL, Mohiuddin U (2003) Fragments of the earliest land plants. Nature 425:282–285PubMedCrossRefGoogle Scholar
  124. Wilkinson JR, Spradling KD, Yoder DW, Pirtle IL, Pirtle M (2005) Molecular cloning and analysis of a cotton gene cluster of two genes and two pseudogenes for the PR5 protein osmotin. Physiol Mol Plant Pathol 67:68–82CrossRefGoogle Scholar
  125. Witty M, Harvey WJ (1990) Sensory evaluation of transgenic Solanum tuberosum producing r-thaumatin II. N Z J Crops Hortic Sci 18:77–80Google Scholar
  126. Yeh S, Moffatt BA, Griffith M, Xiong F, Yang DSC, Wiseman SB, Sarhan F, Danyluk J, Xue YQ, Hew CL, Doherty-Kirby A, Lajoie G (2000) Chitinase genes responsive to cold encode antifreeze proteins in winter cereals. Plant Physiol 124:1251–1264PubMedCrossRefGoogle Scholar
  127. Yu XM, Griffith M (1999) Antifreeze proteins in winter rye leaves form oligomeric complexes. Plant Physiol 119:1361–1369PubMedCrossRefGoogle Scholar
  128. Yu XM, Griffith M (2001) Winter rye antifreeze activity increases in response to cold and drought, but not abscisic acid. Physiol Plant 112:78–86PubMedCrossRefGoogle Scholar
  129. Yu XM, Griffith M, Wiseman SB (2001) Ethylene induces antifreeze activity in winter rye leaves. Plant Physiol 126:1232–1240PubMedCrossRefGoogle Scholar
  130. Yun D-J, 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 1:807–817PubMedCrossRefGoogle Scholar
  131. Yun D-J, Zhao Y, Pardo JM, Narasimhan ML, Damsz B, Lee H, Abad LR, D’Urzo MP, Hasegawa PM, Bressan RA (1997) Stress proteins on the yeast cell surface determine resistance to osmotin, a plant antifungal protein. Proc Natl Acad Sci USA 94:7082–7087PubMedCrossRefGoogle Scholar
  132. Zamani A, Sturrock RN, Ekramoddoullah AKM, Liu J-J, Yu X (2004) Gene cloning and tissue expression analysis of a PR-5 thaumatin-like protein in Phellinus weirii infected Douglas-fir. Phytopathology 94:1235–1243PubMedCrossRefGoogle Scholar
  133. Zareie R, Melanson DL, Murphy PJ (2002) Isolation of fungal cell wall degrading proteins from barley (Hordeum vulgare L.) leaves infected with Rhynchosporium secalis. Mol Plant-Microbe Interact 15:1031–1039PubMedCrossRefGoogle Scholar
  134. Zawirska-Wojtasiak R, Gośliński M, Szwacka M, Gajc-Wolska J, Mildner-Szkudlarz S (2009) Aroma evaluation of transgenic, thaumatin II-producing cucumber fruits. J Food Sci 74(3):C204–C210PubMedCrossRefGoogle Scholar
  135. Zemanek EC, Wasserman BP (1995) Issues and advances in the use of transgenic organisms for the production of thaumatin, the intensely sweet protein from Thaumatococcus danielli. Crit Rev Food Sci Nutr 35:455–466PubMedCrossRefGoogle Scholar

Copyright information

© Her Majesty the Queen in Rights of Canada 2010

Authors and Affiliations

  • Jun-Jun Liu
    • 1
    Email author
  • Rona Sturrock
    • 1
  • Abul K. M. Ekramoddoullah
    • 1
  1. 1.Natural Resources Canada, Canadian Forest ServicePacific Forestry CentreVictoriaCanada

Personalised recommendations