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

  • Lee, Ok-Ran (Korean Ginseng Center for Most Valuable Products & Ginseng Genetic Resource Bank, Kyung Hee University) ;
  • Sathiyaraj, Gayathri (Korean Ginseng Center for Most Valuable Products & Ginseng Genetic Resource Bank, Kyung Hee University) ;
  • Kim, Yu-Jin (Korean Ginseng Center for Most Valuable Products & Ginseng Genetic Resource Bank, Kyung Hee University) ;
  • In, Jun-Gyo (Korean Ginseng Center for Most Valuable Products & Ginseng Genetic Resource Bank, Kyung Hee University) ;
  • Kwon, Woo-Seang (Korean Ginseng Center for Most Valuable Products & Ginseng Genetic Resource Bank, Kyung Hee University) ;
  • Kim, Ju-Han (Korean Ginseng Center for Most Valuable Products & Ginseng Genetic Resource Bank, Kyung Hee University) ;
  • Yang, Deok-Chun (Korean Ginseng Center for Most Valuable Products & Ginseng Genetic Resource Bank, Kyung Hee University)
  • Received : 2010.08.16
  • Accepted : 2010.11.01
  • Published : 2011.03.29

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 fitness. We hypothesize that ginseng, as with other plants, possesses regulatory mechanisms that coordinate the activation of attacker-specific defenses in order to minimize fitness 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 specific 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.

Keywords

References

  1. Cho JS, Han YN, Oh HI, Park H, Sung HS, Park JI. Understanding of Korean ginseng: Korean ginseng contains various effective components. Seoul: The Society for Korean Ginseng, 1995.
  2. Lee FC. Facts about ginseng: the elixir of life. Elizabeth: Hollym International Corp., 1992.
  3. See DM, Broumand N, Sahl L, Tilles JG. 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. Immunopharmacology 1997;35:229-235. https://doi.org/10.1016/S0162-3109(96)00125-7
  4. Song Z, Johansen HK, Faber V, Moser C, Kharazmi A, Rygaard J, Hoiby N. Ginseng treatment reduces bacterial load and lung pathology in chronic Pseudomonas aeruginosa pneumonia in rats. Antimicrob Agents Chemother 1997;41:961-964.
  5. Nishiyama N, Chu PJ, Saito H. An herbal prescription, S-113m, consisting of biota, ginseng and schizandra, improves learning performance in senescence accelerated mouse. Biol Pharm Bull 1996;19:388-393. https://doi.org/10.1248/bpb.19.388
  6. Scaglione F, Cattaneo G, Alessandria M, Cogo R. Efficacy and safety of the standardised Ginseng extract G115 for potentiating vaccination against the influenza syndrome and protection against the common cold [corrected]. Drugs Exp Clin Res 1996;22:65-72.
  7. Kin HS, Kang JG, Oh KW. Inhibition by ginseng total saponin of the development of morphine reverse tolerance and dopamine receptor supersensitivity in mice. Gen Pharmacol 1995;26:1071-1076. https://doi.org/10.1016/0306-3623(94)00267-Q
  8. Kim H, Chen X, Gillis CN. Ginsenosides protect pulmonary vascular endothelium against free radical-induced injury. Biochem Biophys Res Commun 1992;189:670-676. https://doi.org/10.1016/0006-291X(92)92253-T
  9. Takahashi M, Tokuyama S, Kaneto H. Anti-stress effect of ginseng on the inhibition of the development of morphine tolerance in stressed mice. Jpn J Pharmacol 1992;59:399-404. https://doi.org/10.1254/jjp.59.399
  10. Rhee YH, Ahn JH, Choe J, Kang KW, Joe C. Inhibition of mutagenesis and transformation by root extracts of Panax ginseng in vitro. Planta Med 1991;57:125-128. https://doi.org/10.1055/s-2006-960047
  11. Takemoto Y, Ueyama T, Saito H, Horio S, Sanada S, Shoji J, Yahara S, Tanaka O, Shibata S. Potentiation of nerve growth factor-mediated nerve fiber production in organ cultures of chicken embryonic ganglia by ginseng saponins: structure-activity relationship. Chem Pharm Bull (Tokyo) 1984;32:3128-3133. https://doi.org/10.1248/cpb.32.3128
  12. Han BH, Han YN, Park MH. Chemical and biochemical studies on antioxidant components of ginseng. In: Chang HM, Yeung HW, Tso WW, Koo A. Advances in Chinese medicinal materials research. Philadelphia: World Scientific Press, 1985. p.485-498.
  13. Khan NA, Singh S. Abiotic stress and plant responses. New Delhi: International Pub House, 2007.
  14. Heath MC, Nimchuk ZL, Xu H. Plant nuclear migrations as indicators of critical interactions between resistant or susceptible cowpea epidermal cells and invasion hyphae of the cowpea rust fungus. New Phytol 1997;135:689-700. https://doi.org/10.1046/j.1469-8137.1997.00710.x
  15. Bolwell GP. Role of active oxygen species and NO in plant defence responses. Curr Opin Plant Biol 1999;2:287-294. https://doi.org/10.1016/S1369-5266(99)80051-X
  16. Hammond-Kosack KE, Jones JD. Resistance gene-dependent plant defense responses. Plant Cell 1996;8:1773-1791. https://doi.org/10.1105/tpc.8.10.1773
  17. Shao HB, Chu LY, Zhao CX, Guo QJ, Liu XA, Ribaut JM. Plant gene regulatory network system under abiotic stress. Acta Biologica Szegediensis 2006;50:1-9.
  18. Ferreira RB, Monteiro S, Freitas R, Santos CN, Chen Z, Batista LM, Duarte J, Borges A, Teixeira AR. The role of plant defence proteins in fungal pathogenesis. Mol Plant Pathol 2007;8:677-700. https://doi.org/10.1111/j.1364-3703.2007.00419.x
  19. van Loon LC. Occurrence and properties of plant pathogenesis-related proteins. In: Datta SK, Muthukrishnan S, eds. Pathogenesis-related proteins in plants. Boca Raton: CRC Press, 1999. p.1-19.
  20. van Loon LC, Rep M, Pieterse CM. Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 2006;44:135-62. https://doi.org/10.1146/annurev.phyto.44.070505.143425
  21. Kim MK, Lee BS, In JG, Sun H, Yoon JH, Yang DC. Comparative analysis of expressed sequence tags (ESTs) of ginseng leaf. Plant Cell Rep 2006;25:599-606. https://doi.org/10.1007/s00299-005-0095-0
  22. van Loon LC, Pierpoint WS, Boller T, Conejero V. Recommendations for naming plant pathogenesis-related proteins. Plant Mol Biol Report 1994;12:245-264. https://doi.org/10.1007/BF02668748
  23. van Loon LC, van Kammen A. Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. “Samsun” and “Samsun NN”. II. Changes in protein constitution after infection with tobacco mosaic virus. Virology 1970;40:190-211.
  24. van Loon LC. Pathogenesis-related proteins. Plant Mol Biol 1985;4:111-116. https://doi.org/10.1007/BF02418757
  25. van Loon LC, van Strien EA. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 1999;55:85-97. https://doi.org/10.1006/pmpp.1999.0213
  26. Leubner-Metzger G, Meins F Jr. Functions and regulation of plant $\beta$-1,3-glucanases (PR-2). In: Datta SK, Muthukrishnan S, eds. Boca Raton: CRC Press, 1999. p.49-76.
  27. Simmons CR, Litts JC, Huang N, Rodriguez RL. Structure of a rice beta-glucanase gene regulated by ethylene, cytokinin, wounding, salicylic acid and fungal elicitors. Plant Mol Biol 1992;18:33-45. https://doi.org/10.1007/BF00018454
  28. Wubben JP, Lawrence CB, de Wit PJ. Differential induction of chitinase and 1,3-$\beta$-glucanase gene expression in tomato by Cladosporium fulvum and its race-specifi c elicitors. Physiol Mol Plant Pathol 1996;48:105-116. https://doi.org/10.1006/pmpp.1996.0010
  29. Kiselev KV, Kusaykin MI, Dubrovina AS, Bezverbny DA, Zvyagintseva TN, Bulgakov VP. The rolC gene induces expression of a pathogenesis-related beta-1,3-glucanase in transformed ginseng cells. Phytochemistry 2006;67:2225-2231. https://doi.org/10.1016/j.phytochem.2006.07.019
  30. Linthorst HJ, Melchers LS, Mayer A, van Roekel JS, Cornelissen BJ, Bol JF. Analysis of gene families encoding acidic and basic beta-1,3-glucanases of tobacco. Proc Natl Acad Sci USA 1990;87:8756-8760. https://doi.org/10.1073/pnas.87.22.8756
  31. Hennig J, Dewey RE, Cutt JR, Klessig DF. Pathogen, salicylic acid and developmental dependent expression of a beta-1,3-glucanase/GUS gene fusion in transgenic tobacco plants. Plant J 1993;4:481-493. https://doi.org/10.1046/j.1365-313X.1993.04030481.x
  32. Dong X, Mindrinos M, Davis KR, Ausubel FM. Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell 1991;3:61-72. https://doi.org/10.1105/tpc.3.1.61
  33. Broekaert WF, Terras FR, Cammue BP. Induced and preformed antimicrobial proteins. In: Slusarenko AJ, Fraser RS, van Loon LC, eds. Mechanisms of resistance to plant diseases. Boston: Kluwer Academic Publishers, 2000. p.371-477.
  34. Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K. Plant chitinases. Plant J 1993;3:31-40. https://doi.org/10.1046/j.1365-313X.1993.t01-1-00999.x
  35. Pulla RK, Lee OR, In JG, Parvin S, Kim YJ, Shim JS, Sun H, Kim YJ, Senthil K, Yang DC. Identifi cation and characterization of class I chitinase in Panax ginseng C. A. Meyer. Mol Biol Rep 2011;38:95-102. https://doi.org/10.1007/s11033-010-0082-6
  36. Bravo JM, Campo S, Murillo I, Coca M, San Segundo B. Fungus- and wound-induced accumulation of mRNA containing a class II chitinase of the pathogenesis-related protein 4 (PR-4) family of maize. Plant Mol Biol 2003;52:745-759. https://doi.org/10.1023/A:1025016416951
  37. Kasprzewska A. Plant chitinases: regulation and function. Cell Mol Biol Lett 2003;8:809-824.
  38. Dudler R, Mauch F, Reimmann C. Thaumatin-like proteins. In: Witty M, Higginbotham JD, eds. Thaumatin. Boca Raton: CRC Press, 1994. p.193-199.
  39. van der Wel H, Loeve K. Isolation and characterization of thaumatin I and II, the sweet-tasting proteins from Thaumatococcus daniellii Benth. Eur J Biochem 1972;31:221-225. https://doi.org/10.1111/j.1432-1033.1972.tb02522.x
  40. Vigers AJ, Roberts WK, Selitrennikoff CP. A new family of plant antifungal proteins. Mol Plant Microbe Interact 1991;4:315-323. https://doi.org/10.1094/MPMI-4-315
  41. Salzman RA, Tikhonova I, Bordelon BP, Hasegawa PM, Bressan RA. Coordinate accumulation of antifungal proteins and hexoses constitutes a developmentally controlled defense response during fruit ripening in grape. Plant Physiol 1998;117:465-472. https://doi.org/10.1104/pp.117.2.465
  42. Singh NK, Bracker CA, Hasegawa PM, Handa AK, Buckel S, Hermodson MA, Pfankoch E, Regnier FE, Bressan RA. Characterization of osmotin: a thaumatin-like protein associated with osmotic adaptation in plant cells. Plant Physiol 1987;85:529-536. https://doi.org/10.1104/pp.85.2.529
  43. Zhu B, Chen TH, Li PH. Expression of three osmotin-like protein genes in response to osmotic stress and fungal infection in potato. Plant Mol Biol 1995;28:17-26. https://doi.org/10.1007/BF00042034
  44. Zhu B, Chen TH, Li PH. Expression of an ABA-responsive osmotin-like gene during the induction of freezing tolerance in Solanum commersonii. Plant Mol Biol 1993;21:729-735. https://doi.org/10.1007/BF00014558
  45. Kim YJ, Lee JH, Jung DY, Sathiyaraj G, Shim JS, In JG, Yang DC. Isolation and characterization of pathogenesisrelated protein 5 (PgPR5) gene from Panax ginseng. Plant Pathol J 2009;25:400-407. https://doi.org/10.5423/PPJ.2009.25.4.400
  46. Laskowski M Jr, Kato I. Protein inhibitors of proteinases. Annu Rev Biochem 1980;49:593-626. https://doi.org/10.1146/annurev.bi.49.070180.003113
  47. Ryan CA. Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu Rev Phytopathol 1990;28:425-449. https://doi.org/10.1146/annurev.py.28.090190.002233
  48. Ryan CA. Proteinase inhibitor gene families: strategies for transformation to improve plant defenses against herbivores. Bioessays 1989;10:20-24. https://doi.org/10.1002/bies.950100106
  49. Williamson VM, Hussey RS. Nematode pathogenesis and resistance in plants. Plant Cell 1996;8:1735-1745. https://doi.org/10.1105/tpc.8.10.1735
  50. Dunaevskii YE, Gladysheva IP, Pavlukova EB, Beliakova GA, Gladyschev DP, Papisova AI, Larionova NI, Belozerrsky MA. The anionic protease inhibitor BBWI-1 from buckwheat seeds. Kinetic properties and possible biological role. Physiol Plant 1997;100:483-488.
  51. Joshi BN, Sainani MN, Bastawade KB, Gupta VS, Ranjekar PK. Cysteine protease inhibitor from pearl millet: a new class of antifungal protein. Biochem Biophys Res Commun 1998;246:382-387. https://doi.org/10.1006/bbrc.1998.8625
  52. Koiwa H, Bressan RA, Hasegawah PM. Regulation of protease inhibitors and plant defense. Trend Plant Sci 1997;2:379-384. https://doi.org/10.1016/S1360-1385(97)90052-2
  53. Ryan CA. Proteolytic enzymes and their inhibitors in plants. Ann Rev Plant Physiol 1973;24:173-196. https://doi.org/10.1146/annurev.pp.24.060173.001133
  54. Jung DY, Lee OR, Kim YJ, Lee JH, Pulla RK, Sathiyaraj G, Shim JS, Yang DC. Molecular characterization of a cysteine proteinase inhibitor, PgCPI, from Panax ginseng C. A. Meyer. Acta Physiol Plant 2010;32:961-970. https://doi.org/10.1007/s11738-010-0485-y
  55. Howe GA, Ryan CA. Suppressors of systemin signaling identify genes in the tomato wound response pathway. Genetics 1999;153:1411-1421.
  56. Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J, et al. The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 2006;18:2999-3014. https://doi.org/10.1105/tpc.106.044107
  57. Lorito M, Broadway RM, Hayes CK, Woo SL, Noviello C, Williams DL, Harman GE. Proteinase inhibitors from plants as a novel class of fungicides. Mol Plant Microbe Interact 1994;7:525-527. https://doi.org/10.1094/MPMI-7-0525
  58. Walter MH, Liu JW, Grand C, Lamb CJ, Hess D. Bean pathogenesis-related (PR) proteins deduced from elicitorinduced transcripts are members of a ubiquitous new class of conserved PR proteins including pollen allergens. Mol Gen Genet 1990;222:353-360. https://doi.org/10.1007/BF00633840
  59. Sikorski M, Handschuh L, Biesiadka J, Legocki AB. Two subclasses of yellow lupine PR10 proteins and their possible function during the symbiosis development. Curr Plant Sci Biotech Agric 2002;38:319-322. https://doi.org/10.1007/0-306-47615-0_171
  60. Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y, Sekimata K, Takatsuto S, Yamaguchi I, Yoshida S. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J 2003;33:887-898. https://doi.org/10.1046/j.1365-313X.2003.01675.x
  61. Jain S, Srivastava S, Sarin NB, Kav NN. Proteomics reveals elevated levels of PR 10 proteins in saline-tolerant peanut (Arachis hypogaea) calli. Plant Physiol Biochem 2006;44:253-259. https://doi.org/10.1016/j.plaphy.2006.04.006
  62. Liu X, Huang B, Lin J, Fei J, Chen Z, Pang Y, Sun X, Tang K. A novel pathogenesis-related protein (SsPR10) from Solanum surattense with ribonucleolytic and antimicrobial activity is stress- and pathogen-inducible. J Plant Physiol 2006;163:546-556. https://doi.org/10.1016/j.jplph.2005.04.031
  63. Somssich IE, Schmelzer E, Kawalleck P, Hahlbrock K. Gene structure and in situ transcript localization of pathogenesis-related protein 1 in parsley. Mol Gen Genet 1988;213:93-98. https://doi.org/10.1007/BF00333403
  64. Moiseyev GP, Fedoreyeva LI, Zhuravlev YN, Yasnetskaya E, Jekel PA, Beintema JJ. Primary structures of two ribonucleases from ginseng calluses. New members of the PR-10 family of intracellular pathogenesis-related plant proteins. FEBS Lett 1997;407:207-210. https://doi.org/10.1016/S0014-5793(97)00337-2
  65. Bufe A, Spangfort MD, Kahlert H, Schlaak M, Becker WM. The major birch pollen allergen, Bet v 1, shows ribonuclease activity. Planta 1996;199:413-415.
  66. Bantignies B, Seguin J, Muzac I, Dedaldechamp F, Gulick P, Ibrahim R. Direct evidence for ribonucleolytic activity of a PR-10-like protein from white lupin roots. Plant Mol Biol 2000;42:871-881. https://doi.org/10.1023/A:1006475303115
  67. Wu F, Yan M, Li Y, Chang S, Song X, Zhou Z, Gong W. cDNA cloning, expression, and mutagenesis of a PR-10 protein SPE-16 from the seeds of Pachyrrhizus erosus. Biochem Biophys Res Commun 2003;312:761-766. https://doi.org/10.1016/j.bbrc.2003.10.181
  68. Pulla RK, Lee OR, In JG, Kim YJ, Senthil K , Yang DC. Expression and functional characterization of pathogenesisrelated protein family 10 gene, PgPR10-2, from Panax ginseng C.A. Meyer. Physiol Mol Plant Pathol 2010;74:323-329. https://doi.org/10.1016/j.pmpp.2010.05.001
  69. Weurman C. Pectinase inhibitors in pears. Acta Bot Neerl 1953;2:107-121. https://doi.org/10.1111/j.1438-8677.1953.tb00269.x
  70. Cervone F, Castoria R, Leckie F, De Lorenzo G. Perception of fungal elicitors and signal transduction. In: Aducci P. Signal transduction in plants. Basel: Birkauser Verlag, 1997. p.53-177.
  71. Favaron F, Castiglioni C, D’Ovidio R, Alghisi P. Polygalacturonase- inhibiting proteins from Allium porrum L. and their role in plant tissue against fungal endopolygalacturonase. Physiol Mol Plant Pathol 1997;50:403-414. https://doi.org/10.1006/pmpp.1997.0099
  72. Cervone F, Hahn MG, De Lorenzo G, Darvill A, Albersheim P. Host-Pathogen Interactions: XXXIII. A plant protein converts a fungal pathogenesis factor into an elicitor of plant defense responses. Plant Physiol 1989;90:542-548. https://doi.org/10.1104/pp.90.2.542
  73. Federici L, Caprari C, Mattei B, Savino C, Di Matteo A, De Lorenzo G, Cervone F, Tsernoglou D. Structural requirements of endopolygalacturonase for the interaction with PGIP (polygalacturonase-inhibiting protein). Proc Natl Acad Sci U S A 2001;98:13425-13430. https://doi.org/10.1073/pnas.231473698
  74. Mattei B, Bernalda MS, Federici L, Roepstorff P, Cervone F, Boffi A. Secondary structure and post-translational modifications of the leucine-rich repeat protein PGIP (polygalacturonase- inhibiting protein) from Phaseolus vulgaris. Biochemistry 2001;40:569-576. https://doi.org/10.1021/bi0017632
  75. Ferrari S, Vairo D, Ausubel FM, Cervone F, De Lorenzo G. Tandemly duplicated Arabidopsis genes that encode polygalacturonase-inhibiting proteins are regulated coordinately by different signal transduction pathways in response to fungal infection. Plant Cell 2003;15:93-106. https://doi.org/10.1105/tpc.005165
  76. Manfredini C, Sicilia F, Ferrari S, Pontiggia D, Salvi G, Caprari C, Lorito M, De Lorenzo G. Polygalacturonaseinhibiting protein 2 of Phaseolus vulgaris inhibits BcPG1, a polygalacturonase of Botrytis cinerea important for pathogenicity, and protects transgenic plants from infection. Physiol Mol Plant Pathol 2005;67:108-115. https://doi.org/10.1016/j.pmpp.2005.10.002
  77. Sathiyaraj G, Srinivasan S, Subramanium S, Kim YJ, Kim YJ, Kwon WS, Yang DC. Polygalacturonase inhibiting protein: isolation, developmental regulation and pathogen related expression in Panax ginseng C.A. Meyer. Mol Biol Rep 2010;37:3445-3454. https://doi.org/10.1007/s11033-009-9936-1
  78. De Lorenzo G, D’Ovidio R, Cervone F. The role of polygalacturonase- inhibiting proteins (PGIPs) in defense against pathogenic fungi. Annu Rev Phytopathol 2001;39:313-335. https://doi.org/10.1146/annurev.phyto.39.1.313
  79. Federici L, Di Matteo A, Fernandez-Recio J, Tsernoglou D, Cervone F. Polygalacturonase inhibiting proteins: players in plant innate immunity? Trends Plant Sci 2006;11:65-70. https://doi.org/10.1016/j.tplants.2005.12.005
  80. Mehli L, Schaart JG, Kjellsen TD, Tran DH, Salentijn EM, Schouten H, Iversen TH. A gene encoding a polygalacturonase- inhibiting protein (PGIP) shows developmental regulation and pathogen-induced expression in strawberry. New Phytol 2004;163:99-110. https://doi.org/10.1111/j.1469-8137.2004.01088.x
  81. Machinandiarena MF, Olivieri FP, Daleo GR, Oliva CR. Isolation and characterization of a polygalacturonaseinhibiting proteins from potato leaves. Accumulation in response tosalicylic acid, wounding and infection. Plant Physiol Biochem 2001;39:129-136. https://doi.org/10.1016/S0981-9428(00)01228-6
  82. Stotz HU, Powell AL, Damon SE, Greve LC, Bennett AB, Labavitch JM. Molecular characterization of a polygalacturonase inhibitor from Pyrus communis L. cv Bartlett. Plant Physiol 1993;102:133-138. https://doi.org/10.1104/pp.102.1.133
  83. Yao C, Conway WS, Sams CE. Purifi cation and characterization of a polygalacturonase-inhibiting protein from apple fruit. Phytopathology 1995;85:1373-1377. https://doi.org/10.1094/Phyto-85-1373
  84. Noctor G. Arisi AM, Jouanin L, Kunert KJ, Rennenberg H, Foyer CH. Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 1998;49:623-647. https://doi.org/10.1093/jexbot/49.321.623
  85. Mannervik B, Alin P, Guthenberg C, Jensson H, Tahir MK, Warholm M, Jornvall H. Identifi cation of three classes of cytosolic glutathione transferase common to several mammalian species: correlation between structural data and enzymatic properties. Proc Natl Acad Sci U S A 1985;82:7202-7206. https://doi.org/10.1073/pnas.82.21.7202
  86. Droog F, Hooykaas P, Van Der Zaal BJ. 2,4-Dichlorophenoxyacetic acid and related chlorinated compounds inhibit two auxin-regulated type-III tobacco glutathione S-transferases. Plant Physiol 1995;107:1139-1146. https://doi.org/10.1104/pp.107.4.1139
  87. Edwards R, Dixon DP, Walbot V. Plant glutathione Stransferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 2000;5:193-198. https://doi.org/10.1016/S1360-1385(00)01601-0
  88. Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 1998;92:773-784. https://doi.org/10.1016/S0092-8674(00)81405-1
  89. Jwa NS, Agrawal GK, Tamogami S, Yonekura M, Han O, Iwahashi H, Rakwal R. Role of defense/stress-related marker genes, proteins and secondary metabolites in defi ning rice self-defense mechanisms. Plant Physiol Biochem 2006;44:261-273. https://doi.org/10.1016/j.plaphy.2006.06.010
  90. Yu L, Kalla K, Guthrie E, Vidrine A, Klimecki WT. Genetic variation in genes associated with arsenic metabolism: glutathione S-transferase omega 1-1 and purine nucleoside phosphorylase polymorphisms in European and indigenous Americans. Environ Health Perspect 2003;111:1421-1427. https://doi.org/10.1289/ehp.6420
  91. Evan PT, Malmberg RL. Do polyamines have roles in plant development? Annu Rev Plant Physiol Plant Mol Biol 1989;40:235-269. https://doi.org/10.1146/annurev.pp.40.060189.001315
  92. Hashimoto T, Tamaki K, Suzuki K, Yamada Y. Molecular cloning of plant spermidine synthases. Plant Cell Physiol 1998;39:73-79. https://doi.org/10.1093/oxfordjournals.pcp.a029291
  93. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J. Polyamines and environmental challenges: recent development. Plant Sci 1999;140:103-125. https://doi.org/10.1016/S0168-9452(98)00218-0
  94. Parvin S, Kim YJ, Pulla RK, Sathiyamoorthy S, Miah MG, Kim YJ, Wasnik NG, Yang DC. Identification and characterization of spermidine synthase gene from Panax ginseng. Mol Biol Rep 2010;37:923-932. https://doi.org/10.1007/s11033-009-9725-x
  95. Shen W, Nada K, Tachibana S. Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiol 2000;124:431-439. https://doi.org/10.1104/pp.124.1.431
  96. Alabadi D, Carbonell J. Molecular cloning and characterization of a tomato (Lycopersicon esculentum Mill.) spermidine synthase cDNA. Plant Physiol 1999;120:935.
  97. Hanzawa Y, Imai A, Michael AJ, Komeda Y, Takahashi T. Characterization of the spermidine synthase-related gene family in Arabidopsis thaliana. FEBS Lett 2002;527:176-180. https://doi.org/10.1016/S0014-5793(02)03217-9
  98. Wang Q, Yuan G, Sun H, Zhao P, Liu Y, Guo D. Molecular cloning and expression analysis of spermidine synthase gene during sex reversal induced by Ethrel in cucumber (Cucumis sativus L.). Plant Sci 2005;169:768-775. https://doi.org/10.1016/j.plantsci.2005.05.032
  99. Jimenez-Bremont JF, Becerra-Flora A, Hernandez-Lucero E, Rodriguez-Kessler M, Acosta-Gallegos J, Ramirez- Pimentel J. Proline accumulation in two bean cultivars under salt stress and the effect of polyamines and ornithine. Biol Plant 2006;50:763-766. https://doi.org/10.1007/s10535-006-0126-x
  100. Roussos PA, Pontikis CA. Changes of free, soluble conjugated and bound polyamine titers of jojoba explants under sodium chloride salinity in vitro. J Plant Physiol 2007;164:895-903. https://doi.org/10.1016/j.jplph.2006.05.003
  101. Shabala S, Cuin TA, Prismall L, Nemchinov LG. Expression of animal CED-9 anti-apoptotic gene in tobacco modifi es plasma membrane ion fl uxes in response to salinity and oxidative stress. Planta 2007;227:189-197. https://doi.org/10.1007/s00425-007-0606-z
  102. Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael AJ, Kusano T. A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun 2007;352:486-490. https://doi.org/10.1016/j.bbrc.2006.11.041
  103. Nessler CL, Allen RD, Galewsky S. Identifi cation and characterization of latex-specific proteins in opium poppy. Plant Physiol 1985;79:499-504. https://doi.org/10.1104/pp.79.2.499
  104. Nessler CL, Kurz WG, Pelcher LE. Isolation and analysis of the major latex protein genes of opium poppy. Plant Mol Biol 1990;15:951-953. https://doi.org/10.1007/BF00039436
  105. Sun H, Kim MK, Pulla RK, Kim YJ, Yang DC. Isolation and expression analysis of a novel major latex-like protein (MLP151) gene from Panax ginseng. Mol Biol Rep 2010;37:2215-2222. https://doi.org/10.1007/s11033-009-9707-z
  106. Osmark P, Boyle B, Brisson N. Sequential and structural homology between intracellular pathogenesis-related proteins and a group of latex proteins. Plant Mol Biol 1998;38:1243-1246. https://doi.org/10.1023/A:1006060224012
  107. Flores T, Alape-Giron A, Flores-Diaz M, Flores HE. Ocatin. A novel tuber storage protein from the andean tuber crop oca with antibacterial and antifungal activities. Plant Physiol 2002;128:1291-1302. https://doi.org/10.1104/pp.010541
  108. MacGregor AJ, Gallimore JR, Spector TD, Pepys MB. Genetic effects on baseline values of C-reactive protein and serum amyloid a protein: a comparison of monozygotic and dizygotic twins. Clin Chem 2004;50:130-134. https://doi.org/10.1373/clinchem.2003.028258
  109. Bown AW, Shelp BJ. The Metabolism and functions of [gamma]-aminobutyric acid. Plant Physiol 1997;115:1-5. https://doi.org/10.1104/pp.115.1.1
  110. Baum G, Chen Y, Arazi T, Takatsuji H, Fromm H. A plant glutamate decarboxylase containing a calmodulin binding domain. Cloning, sequence, and functional analysis. J Biol Chem 1993;268:19610-19617.
  111. Arazi T, Baum G, Snedden WA, Shelp BJ, Fromm H. Molecular and biochemical analysis of calmodulin interactions with the calmodulin-binding domain of plant glutamate decarboxylase. Plant Physiol 1995;108:551-561. https://doi.org/10.1104/pp.108.2.551
  112. Lee JH, Kim YJ, Jeong DY, Sathiyaraj G, Pulla RK, Shim JS, In JG, Yang DC. Isolation and characterization of a Glutamate decarboxylase (GAD) gene and their differential expression in response to abiotic stresses from Panax ginseng C. A. Meyer. Mol Biol Rep 2010;37:3455-3463. https://doi.org/10.1007/s11033-009-9937-0
  113. Sanders D, Brownlee C, Harper JF. Communicating with calcium. Plant Cell 1999;11;691-706. https://doi.org/10.1105/tpc.11.4.691
  114. Snedden WA, Fromm H. Regulation of the c-aminobutyrate- synthesizing enzyme, glutamate decarboxylase, by calcium-calmodulin: a mechanism for rapid activation in response to stress. In: Lerner HR, ed. Plant responses to environmental stresses: from phytohormones to genome reorganization. New York: Marcel Dekker, 1999. p. 549.
  115. Fromm H, Snedden WA. Role of $Ca^{2+}$/calmodulin in plant response to abiotic stresses: a review. Acta Hort (ISHS) 1997;447:431-438.
  116. Kaplan F, Kopka J, Sung DY, Zhao W, Popp M, Porat R, Guy CL. Transcript and metabolite profi ling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 2007;50:967-981. https://doi.org/10.1111/j.1365-313X.2007.03100.x
  117. Wasnik N, Kim YJ, Kim SH, Sathyamoorthy S, Pulla RK, Parvin S, Senthil K, Yang DC. Isolation and characterization of calmodulin gene from Panax ginseng C. A. Meyer. J Ginseng Res 2009;33:59-64. https://doi.org/10.5142/JGR.2009.33.1.059
  118. Purev M, Kim YJ, Kim MK, Pulla RK, Yang DC. Isolation of a novel catalase (Cat1) gene from Panax ginseng and analysis of the response of this gene to various stresses. Plant Physiol Biochem 2010;48(6):451-60. https://doi.org/10.1016/j.plaphy.2010.02.005
  119. Kim YJ. Isolation of glutathione Stransferase gene from Panax ginseng and analysis of its response against environmental stresses [dissertation]. Seoul: Kyung Hee University, 2008.

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