Defense Genes Induced by Pathogens and Abiotic Stresses in Panax ginseng C. A. Meyer

다국어 초록 (Multilingual Abstract)

Korean ginseng is a medicinally important perennial herb from the family Araliaceae. It has been cultivated for its highly valued medicinal properties for over 1,000 years in east Asian countries such as China, Korea, and Japan. Due to its longtime cultivation in shady areas, ginseng is frequently exposed to pathogenic infections. Plants protect themselves from microbial pathogens using an array of defense mechanisms, some of which are constitutively active, while others are activated upon pathogen invasion. These induced defense responses, controlled by defense-related genes, require tradeoffs in terms of plant fi tness. We hypothesize that ginseng, as with other plants, possesses regulatory mechanisms that coordinate the activation of attacker-specifi c defenses in order to minimize fi tness costs while attaining optimal resistance. Several classes of defense-related genes are induced by infection, wounds, irradiation, and other abiotic stresses. Both salicylates and jasmonates have been shown to cause such responses, although their specifi c roles and interactions in signaling and development are not fully understood in ginseng. This review summarizes possible defense-related genes in ginseng based on their expression patterns against biotic and abiotic stresses and describes their functional roles.

목차 (Table of Contents)

• INTRODUCTION
• UNDERSTANDING THE DEFENSE MECHANISMS IN GINSENG
• PATHOGENESIS-RELATED PROTEIN
• PR-LIKE PROTEINS
• OTHER DEFENSE-RELATED GENES
• CONCLUSION
• ACKNOWLEDGEMENTS
• REFERENCES

참고문헌 (Reference)

1 Wu F, "cDNA cloning, expression, and mutagenesis of a PR-10 protein SPE-16 from the seeds of Pachyrrhizus erosus" 312 : 761-766, 2003

2 Cho JS, "Understanding of Korean ginseng: Korean ginseng contains various effective components" The Society for Korean Ginseng 1995

3 Sikorski M, "Two subclasses of yellow lupine PR10 proteins and their possible function during the symbiosis development" 38 : 319-322, 2002

4 Kaplan F, "Transcript and metabolite profi ling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content" 50 : 967-981, 2007

5 De Lorenzo G, "The role of polygalacturonase- inhibiting proteins (PGIPs) in defense against pathogenic fungi" 39 : 313-335, 2001

6 Ferreira RB, "The role of plant defence proteins in fungal pathogenesis" 8 : 677-700, 2007

7 Kiselev KV, "The rolC gene induces expression of a pathogenesis-related beta-1,3-glucanase in transformed ginseng cells" 67 : 2225-2231, 2006

8 Li N, "The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development" 18 : 2999-3014, 2006

9 Bufe A, "The major birch pollen allergen, Bet v 1, shows ribonuclease activity" 199 : 413-415, 1996

10 van Loon LC, "The families of pathogenesis- related proteins, their activities, and comparative analysis of PR-1 type proteins" 55 : 85-97, 1999

11 Dunaevskii YE, "The anionic protease inhibitor BBWI-1 from buckwheat seeds. Kinetic properties and possible biological role" 100 : 483-488, 1997

12 Bown AW, "The Metabolism and functions of [gamma]-aminobutyric acid" 115 : 1-5, 1997

13 Dudler R, "Thaumatin-like proteins, in Thaumatin" CRC Press 193-199, 1994

14 프레드릭, "Tandemly duplicated arabidopsis genes that encode polygalacturonase-inhibiting proteins are regulated coordinately by different signal transduction pathways in response to fungal infection" 15 (15): 93-106, 200301

15 Howe GA, "Suppressors of systemin signaling identify genes in the tomato wound response pathway" 153 : 1411-1421, 1999

16 Simmons CR, "Structure of a rice beta-glucanase gene regulated by ethylene, cytokinin, wounding, salicylic acid and fungal elicitors" 18 : 33-45, 1992

17 Federici L, "Structural requirements of endopolygalacturonase for the interaction with PGIP (polygalacturonase-inhibiting protein)" 98 : 13425-13430, 2001

18 van Loon LC, "Significance of inducible defense-related proteins in infected plants" 44 : 135-162, 2006

19 Osmark P, "Sequential and structural homology between intracellular pathogenesis-related proteins and a group of latex proteins" 38 : 1243-1246, 1998

20 Mattei B, "Secondary structure and post-translational modifications of the leucine-rich repeat protein PGIP (polygalacturonase- inhibiting protein) from Phaseolus vulgaris" 40 : 569-576, 2001

21 한옥수, "Role of defense/stress-related marker genes, proteins and secondary metabolites in defining rice self-defense mechanisms" 44 (44): 261-273, 200606

22 Bolwell GP, "Role of active oxygen species and NO in plant defence responses" 2 : 287-294, 1999

23 Fromm H, "Role of Ca2+/calmodulin in plant response to abiotic stresses: a review" 447 : 431-438, 1997

24 Hammond-Kosack KE, "Resistance gene-dependent plant defense responses" 8 : 1773-1791, 1996

25 Snedden WA, "Regulation of the c-aminobutyrate- synthesizing enzyme, glutamate decarboxylase, by calcium-calmodulin: a mechanism for rapid activation in response to stress, in Plant responses to environmental stresses: from phytohormones to genome reorganization" Marcel Dekker 549-, 1999

26 Koiwa H, "Regulation of protease inhibitors and plant defense" 2 : 379-384, 1997

27 van Loon LC, "Recommendations for naming plant pathogenesis-related proteins" 12 : 245-264, 1994

28 Alvarez ME, "Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity" 92 : 773-784, 1998

29 Yao C, "Purifi cation and characterization of a polygalacturonase-inhibiting protein from apple fruit" 85 : 1373-1377, 1995

30 Jain S, "Proteomics reveals elevated levels of PR 10 proteins in saline-tolerant peanut (Arachis hypogaea) calli" 44 : 253-259, 2006

31 Ryan CA, "Proteolytic enzymes and their inhibitors in plants" 24 : 173-196, 1973

32 Lorito M, "Proteinase inhibitors from plants as a novel class of fungicides" 7 : 525-527, 1994

33 Ryan CA, "Proteinase inhibitor gene families: strategies for transformation to improve plant defenses against herbivores" 10 : 20-24, 1989

34 Laskowski M Jr, "Protein inhibitors of proteinases" 49 : 593-626, 1980

35 Ryan CA, "Protease inhibitors in plants: genes for improving defenses against insects and pathogens" 28 : 425-449, 1990

36 Jimenez-Bremont JF, "Proline accumulation in two bean cultivars under salt stress and the effect of polyamines and ornithine" 50 : 763-766, 2006

37 Moiseyev GP, "Primary structures of two ribonucleases from ginseng calluses. New members of the PR-10 family of intracellular pathogenesis-related plant proteins" 407 : 207-210, 1997

38 Takemoto Y, "Potentiation of nerve growth factor-mediated nerve fiber production in organ cultures of chicken embryonic ganglia by ginseng saponins: structure-activity relationship" 32 : 3128-3133, 1984

39 Manfredini C, "Polygalacturonaseinhibiting protein 2 of Phaseolus vulgaris inhibits BcPG1, a polygalacturonase of Botrytis cinerea important for pathogenicity, and protects transgenic plants from infection" 67 : 108-115, 2005

40 Favaron F, "Polygalacturonase- inhibiting proteins from Allium porrum L. and their role in plant tissue against fungal endopolygalacturonase" 50 : 403-414, 1997

41 Federici L, "Polygalacturonase inhibiting proteins: players in plant innate immunity" 11 : 65-70, 2006

42 Sathiyaraj G, "Polygalacturonase inhibiting protein: isolation, developmental regulation and pathogen related expression in Panax ginseng C.A. Meyer" 37 : 3445-3454, 2010

43 Bouchereau A, "Polyamines and environmental challenges: recent development" 140 : 103-125, 1999

44 van Loon LC, "Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. “Samsun” and “Samsun NN”. II. Changes in protein constitution after infection with tobacco mosaic virus" 40 : 190-211, 1970

45 Heath MC, "Plant nuclear migrations as indicators of critical interactions between resistant or susceptible cowpea epidermal cells and invasion hyphae of the cowpea rust fungus" 135 : 689-700, 1997

46 Edwards R, "Plant glutathione Stransferases: enzymes with multiple functions in sickness and in health" 5 : 193-198, 2000

47 Shao HB, "Plant gene regulatory network system under abiotic stress" 50 : 1-9, 2006

48 Kasprzewska A, "Plant chitinases: regulation and function" 8 : 809-824, 2003

49 Collinge DB, "Plant chitinases" 3 : 31-40, 1993

50 Cervone F, "Perception of fungal elicitors and signal transduction, in Signal transduction in plants" Birkauser Verlag 53-177, 1997

51 Weurman C, "Pectinase inhibitors in pears" 2 : 107-121, 1953

52 van Loon LC, "Pathogenesis-related proteins" 4 : 111-116, 1985

53 Hennig J, "Pathogen, salicylic acid and developmental dependent expression of a beta-1,3-glucanase/GUS gene fusion in transgenic tobacco plants" 4 : 481-493, 1993

54 van Loon LC, "Occurrence and properties of plant pathogenesis- related proteins, in Pathogenesis-related proteins in plants" CRC Press 1-19, 1999

55 Flores T, "Ocatin. A novel tuber storage protein from the andean tuber crop oca with antibacterial and antifungal activities" 128 : 1291-1302, 2002

56 Williamson VM, "Nematode pathogenesis and resistance in plants" 8 : 1735-1745, 1996

57 Hashimoto T, "Molecular cloning of plant spermidine synthases" 39 : 73-79, 1998

58 Wang Q, "Molecular cloning and expression analysis of spermidine synthase gene during sex reversal induced by Ethrel in cucumber (Cucumis sativus L.)" 169 : 768-775, 2005

59 Alabadi D, "Molecular cloning and characterization of a tomato (Lycopersicon esculentum Mill.) spermidine synthase cDNA" 120 : 935-, 1999

60 Stotz HU, "Molecular characterization of a polygalacturonase inhibitor from Pyrus communis L. cv Bartlett" 102 : 133-138, 1993

61 Jung DY, "Molecular characterization of a cysteine proteinase inhibitor, PgCPI, from Panax ginseng C. A. Meyer" 32 : 961-970, 2010

62 Arazi T, "Molecular and biochemical analysis of calmodulin interactions with the calmodulin-binding domain of plant glutamate decarboxylase" 108 : 551-561, 1995

63 Kim YJ, "Isolation of glutathione Stransferase gene from Panax ginseng and analysis of its response against environmental stresses" Kyung Hee University 2008

64 Purev M, "Isolation of a novel catalase (Cat1) gene from Panax ginseng and analysis of the response of this gene to various stresses" 48 (48): 451-460, 2010

65 Sun H, "Isolation and expression analysis of a novel major latex-like protein (MLP151) gene from Panax ginseng" SPRINGER 37 (37): 2215-2222, 2010

66 van der Wel H, "Isolation and characterization of thaumatin I and II, the sweet-tasting proteins from Thaumatococcus daniellii Benth" 31 : 221-225, 1972

67 Machinandiarena MF, "Isolation and characterization of a polygalacturonaseinhibiting proteins from potato leaves. Accumulation in response tosalicylic acid, wounding and infection" 39 : 129-136, 2001

68 양덕춘, "Isolation and characterization of a Glutamate decarboxylase (GAD) gene and their differential expression in response to abiotic stresses from Panax ginseng C. A. Meyer" 37 (37): 3455-3463, 201010

69 Nessler CL, "Isolation and analysis of the major latex protein genes of opium poppy" 15 : 951-953, 1990

70 김유진, "Isolation and Characterization of Pathogenesis-Related Protein 5 (PgPR5) Gene from Panax ginseng" 한국식물병리학회 25 (25): 400-407, 2009

71 Neha G. Wasnik, "Isolation and Characterization of Calmodulin Gene from Panax ginseng C. A. Meyer" 고려인삼학회 33 (33): 59-64, 2009

72 Shen W, "Involvement of polyamines in the chilling tolerance of cucumber cultivars" 124 : 431-439, 2000

73 Dong X, "Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene" 3 : 61-72, 1991

74 Broekaert WF, "Induced and preformed antimicrobial proteins, in Mechanisms of resistance to plant diseases" Kluwer Academic Publishers 371-477, 2000

75 See DM, "In vitro effects of echinacea and ginseng on natural killer and antibodydependent cell cytotoxicity in healthy subjects and chronic fatigue syndrome or acquired immunodefi ciency syndrome patients" 35 : 229-235, 1997

76 Parvin S, "Identification and characterization of spermidine synthase gene from Panax ginseng" 37 : 923-932, 2010

77 Mannervik B, "Identifi cation of three classes of cytosolic glutathione transferase common to several mammalian species: correlation between structural data and enzymatic properties" 82 : 7202-7206, 1985

78 Nessler CL, "Identifi cation and characterization of latex-specific proteins in opium poppy" 79 : 499-504, 1985

79 Pulla RK, "Identifi cation and characterization of class I chitinase in Panax ginseng C. A. Meyer" 38 : 95-102, 2011

80 조철오, "INHIBITION OF MUTAGENESIS AND TRANSFORMATION BY ROOT EXTRACTS OF PANAX-GINSENG INVITRO" 57 (57): 125-128, 199104

81 오기완, "INHIBITION BY GINSENG TOTAL SAPONIN OF THE DEVELOPMENT OF MORPHINE REVERSE TOLERANCE AND DOPAMINE-RECEPTOR SUPERSENSITIVITY IN MICE" 26 : 1071-1076, 199509

82 Cervone F, "Host-Pathogen Interactions: XXXIII. A plant protein converts a fungal pathogenesis factor into an elicitor of plant defense responses" 90 : 542-548, 1989

83 Noctor G, "Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants" 49 : 623-647, 1998

84 Kim H, "Ginsenosides protect pulmonary vascular endothelium against free radical-induced injury" 189 : 670-676, 1992

85 Song Z, "Ginseng treatment reduces bacterial load and lung pathology in chronic Pseudomonas aeruginosa pneumonia in rats" 41 : 961-964, 1997

86 Yu L, "Genetic variation in genes associated with arsenic metabolism: glutathione S-transferase omega 1-1 and purine nucleoside phosphorylase polymorphisms in European and indigenous Americans" 11 : 1421-1427, 2003

87 MacGregor AJ, "Genetic effects on baseline values of C-reactive protein and serum amyloid a protein: a comparison of monozygotic and dizygotic twins" 50 : 130-134, 2004

88 Somssich IE, "Gene structure and in situ transcript localization of pathogenesis-related protein 1 in parsley" 213 : 93-98, 1988

89 Bravo JM, "Fungus- and wound-induced accumulation of mRNA containing a class II chitinase of the pathogenesis-related protein 4 (PR-4) family of maize" 52 : 745-759, 2003

90 Leubner-Metzger G, "Functions and regulation of plant β-1,3-glucanases (PR-2)" CRC Press 49-76, 1999

91 Lee FC, "Facts about ginseng: the elixir of life" Hollym International Corp 1992

92 Zhu B, "Expression of three osmotin-like protein genes in response to osmotic stress and fungal infection in potato" 28 : 17-26, 1995

93 Shabala S, "Expression of animal CED-9 anti-apoptotic gene in tobacco modifi es plasma membrane ion fl uxes in response to salinity and oxidative stress" 227 : 189-197, 2007

94 Zhu B, "Expression of an ABA-responsive osmotin-like gene during the induction of freezing tolerance in Solanum commersonii" 21 : 729-735, 1993

95 Pulla RK, "Expression and functional characterization of pathogenesisrelated protein family 10 gene, PgPR10-2, from Panax ginseng C.A. Meyer" 74 : 323-329, 2010

96 Scaglione F, "Efficacy and safety of the standardised Ginseng extract G115 for potentiating vaccination against the influenza syndrome and protection against the common cold [corrected]" 22 : 65-72, 1996

97 Evan PT, "Do polyamines have roles in plant development" 40 : 235-269, 1989

98 Bantignies B, "Direct evidence for ribonucleolytic activity of a PR-10-like protein from white lupin roots" 42 : 871-881, 2000

99 Wubben JP, "Differential induction of chitinase and 1,3- β-glucanase gene expression in tomato by Cladosporium fulvum and its race-specifi c elicitors" 48 : 105-116, 1996

100 Joshi BN, "Cysteine protease inhibitor from pearl millet: a new class of antifungal protein" 246 : 382-387, 1998

101 Salzman RA, "Coordinate accumulation of antifungal proteins and hexoses constitutes a developmentally controlled defense response during fruit ripening in grape" 117 : 465-472, 1998

102 Kim MK, "Comparative analysis of expressed sequence tags (ESTs) of ginseng leaf" SPRINGER 25 : 599-606, 2006

103 Sanders D, "Communicating with calcium" 11 : 691-706, 1999

104 Han BH, "Chemical and biochemical studies on antioxidant components of ginseng, in Advances in Chinese medicinal materials research" World Scientifi c Press 485-498, 1985

105 Hanzawa Y, "Characterization of the spermidine synthase-related gene family in Arabidopsis thaliana" 57 : 176-180, 2002

106 Singh NK, "Characterization of osmotin: a thaumatin-like protein associated with osmotic adaptation in plant cells" 85 : 529-536, 1987

107 Roussos PA, "Changes of free, soluble conjugated and bound polyamine titers of jojoba explants under sodium chloride salinity in vitro" 164 : 895-903, 2007

108 Nakashita H, "Brassinosteroid functions in a broad range of disease resistance in tobacco and rice" 33 : 887-898, 2003

109 Walter MH, "Bean pathogenesis-related (PR) proteins deduced from elicitorinduced transcripts are members of a ubiquitous new class of conserved PR proteins including pollen allergens" 222 : 353-360, 1990

110 Takahashi M, "Anti-stress effect of ginseng on the inhibition of the development of morphine tolerance in stressed mice" 59 : 399-404, 1992

111 Linthorst HJ, "Analysis of gene families encoding acidic and basic beta-1,3-glucanases of tobacco" 87 : 8756-8760, 1990

112 Nishiyama N, "An herbal prescription, S-113m, consisting of biota, ginseng and schizandra, improves learning performance in senescence accelerated mouse" 19 : 388-393, 1996

113 Khan NA, "Abiotic stress and plant responses" International Pub House 2007

114 Yamaguchi K, "A protective role for the polyamine spermine against drought stress in Arabidopsis" 352 : 486-490, 2007

115 Baum G, "A plant glutamate decarboxylase containing a calmodulin binding domain. Cloning, sequence, and functional analysis" 268 : 19610-19617, 1993

116 Liu X, "A novel pathogenesis-related protein (SsPR10) from Solanum surattense with ribonucleolytic and antimicrobial activity is stress- and pathogen-inducible" 163 : 546-556, 2006

117 Vigers AJ, "A new family of plant antifungal proteins" 4 : 315-323, 1991

118 Mehli L, "A gene encoding a polygalacturonase- inhibiting protein (PGIP) shows developmental regulation and pathogen-induced expression in strawberry" 163 : 99-110, 2004

119 Droog F, "2,4-Dichlorophenoxyacetic acid and related chlorinated compounds inhibit two auxin-regulated type-III tobacco glutathione S-transferases" 107 : 1139-1146, 1995