Modulation of phytoalexin biosynthesis in engineered plants for disease resistance

International Journal of Molecular Sciences

Volumn 14, Issue 7, 2013, Pages 14136-14170

  Jeandet, Philippe ^a   Clément, Christophe ^a   Courot, Eric ^a   Cordelier, Sylvain ^a  

^a UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

Author keywords

Elicitors; Hormones; Phytoalexins; Plant engineering; Regulation; Transcriptional factors

Indexed keywords

ABSCISIC ACID; COMPLEMENTARY DNA; CYTOKININ; ISOFLAVONE O METHYLTRANSFERASE; ISOFLAVONOID; METHYLTRANSFERASE; MITOGEN ACTIVATED PROTEIN KINASE; PHYTOALEXIN; PHYTOHORMONE; STILBENE DERIVATIVE; UNCLASSIFIED DRUG;

ARABIDOPSIS; BIOACCUMULATION; BIOSYNTHESIS; CHEMICAL STRUCTURE; GENE; GENE FUNCTION; GENE IDENTIFICATION; GENETIC ENGINEERING; GLYCOSYLATION; HORMONAL REGULATION; HUMAN; MOLECULAR DYNAMICS; NONHUMAN; PLANT DEFENSE; PLANT DISEASE; PLANT GENETICS; PLANT METABOLISM; PROTEIN EXPRESSION; REVIEW; RS3 GENE; SIGNAL TRANSDUCTION; STILBENE SYNTHASE GENE; TRANSCRIPTION REGULATION; UPREGULATION; VST1 GENE; VST2 GENE;

DISEASE RESISTANCE; PLANTS; PLANTS, GENETICALLY MODIFIED; SCOPOLETIN; SESQUITERPENES; TOBACCO; TRANSCRIPTION FACTORS;

EID: 84880150874     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140714136     Document Type: Review

References (178)

1. Müller, K.O.; Börger, H. Experimentelle untersuchungen über die Phytophthora resistenz der Kartoffel. Arbeit. Biol. Reichsant Land Forstwirtsch. 1940, 23, 189-231.
2. Deverall, B.J. Introduction. In Phytoalexins; Bailey, J.A., Mansfield, J.W., Eds.; Blackie: Glasgow and London, UK, 1982; pp. 1-20.
3. Mansfield, J.W.; Bailey, J.A. Phytoalexins: Current Problems and Future Prospects. In Phytoalexins; Bailey, J.A., Mansfield, J.W., Eds.; Blackie: Glasgow and London, UK, 1982; pp. 319-323.
4. Ahuja, I.; Kissen, R.; Bones, A.M. Phytoalexins in defense against pathogens. Trends Plant Sci. 2012, 17, 73-90.
5. Thomma, B.P.H.J.; Nelissen, I.; Eggermont, K.; Broekaert, W.F. Deficiency in phytoalexin production causes enhanced susceptibilty of Arabidopsis thaliana to the fungus Alternaria brassicola. Plant J. 1999, 19, 163-171.
6. VanWees, S.C.; Chang, H.S.; Zhu, T.; Glazebrook, J. Characterization of the early response of Arabidopsis to Alternaria brassicicola infection using expression profiling. Plant Physiol. 2003, 132, 606-617.
7. Rowe, H.C.; Walley, J.W.; Corwin, J.; Chan, E.K.F.; Dehesh, K.; Kliebenstein, D.J. Deficiencies in jasmonate-mediated plant defense reveal quantitative variation in Botrytis cinerea pathogenesis. PLoS Pathog. 2010, 6, e1000861.
8. Nawrath, C.; Métraux, J.P. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 1999, 11, 1393-1404.
9. Roetschi, A.; Si-Ammour, A.; Belbahri, L.; Mauch, F.; Mauch-Mani, B. Characterization of an Arabidopsis-Phytophthora pathosystem: Resistance requires a functional PAD2 gene and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J. 2001, 28, 293-305.
10. Denby, K.J.; Jason, L.J.M.; Murray, S.L.; Last, R.L. ups1, an Arabidopsis thaliana camalexin accumulation mutant defective in multiple defence signalling pathways. Plant J. 2005, 41, 673-684.
11. Heck, S.; Grau, T.; Buchala, A.; Métraux, J.P.; Nawrath, C. Genetic evidence that expression of NahG modifies defence pathways independent of salicylic acid biosynthesis in the Arabidopsis-Pseudomonas syringae pv. tomato interaction. Plant J. 2003, 36, 342-352.
12. Robert-Seilaniantz, A.; MacLean, D.; Jikumaru, Y.; Hill, L.; Yamaguchi, S.; Kamiya, Y.; Jones, J.D.G. The microRNA miR393 re-directs secondary metabolite biosynthesis away from camalexin and towards glucosinates. Plant J. 2011, 67, 218-231.
13. Ren, D.; Liu, Y.; Yang, K.Y.; Han, L.; Mao, G.; Glazebrook, J.; Zhang, S. A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc. Natl Acad. Sci. USA 2008, 105, 5638-5643.
14. Pandey, S.P.; Rocarro, M.; Schön, M.; Logemann, E.; Somssich, I.E. Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis. Plant J. 2010, 64, 912-923.
15. Smith, D.A. Toxicity of Phytoalexins. In Phytoalexins; Bailey, J.A., Mansfield, J.W., Eds.; Blackie: Glasgow and London, UK, 1982; pp. 218-252.
16. Rathmell, W.G.; Smith, D.A. Lack of activity of selected isoflavonoid phytoalexins as protectant fungicides. Pestic. Sci. 1980, 11, 568-572.
17. Pezet, R.; Pont, V. Ultrastructural observations of pterostilbene fungitoxicity in dormant conidia of Botrytis cinerea Pers. J. Phytopathol. 1990, 129, 29-30.
18. Adrian, M.; Jeandet, P.; Veneau, J.; Weston, L.A.; Bessis, R. Biological activity of resveratrol, a stilbenic compound from grapevines, against Botrytis cinerea, the causal agent for gray mold. J. Chem. Ecol. 1997, 23, 1689-1702.
19. Adrian, M.; Jeandet, P. Effects of resveratrol on the ultrastructure of Botrytis cinerea conidia and biological significance in plant/pathogen interactions. Fitoterapia 2012, 83, 1345-1350.
20. Shlezinger, N.; Minz, A.; Gur, Y.; Hatam, I.; Dagdas, Y.F.; Talbot, N.J.; Sharon, A. Anti-apoptotic machinery protects the necrotrophic fungus Botrytis cinerea from host-induced apoptotic-like cell death during plant infection. PLoS Pathog. 2011, 7, e1002185.
21. Ingham, J.L. Phytoalexins from the Leguminosae. In Phytoalexins; Bailey, J.A., Mansfield, J.W., Eds.; Blackie: Glasgow and London, UK, 1982; pp. 21-80.
22. Kuc, J. Phytoalexins from the Solanaceae. In Phytoalexins; Bailey, J.A., Mansfield, J.W., Eds.; Blackie: Glasgow and London, UK, 1982; pp. 81-105.
23. Coxon, D.T. Phytoalexins from other Plant Families. In Phytoalexins; Bailey, J.A., Mansfield, J.W., Eds.; Blackie: Glasgow and London, UK, 1982; pp.106-132.
24. Keen, N.T.; Zaki, A.; Sims, J.J. Biosynthesis of hydoxyphaseollin and related isoflavanoids in disease-resistant soybean hypocotyls. Phytochemistry 1972, 11, 1031-1039.
25. Markham, K.R.; Ingham, J.L. Tectorigenin, a phytoalexin from Centrosema haitiense and other Centrosema species. Z. Naturforsch. C 1980, 35, 919-922.
26. Ingham, J.L. Induced isoflavanoids from fungus-infected stems of pigeon pea (Cajanus cajan). Z. Naturforsch. C 1976, 31, 504-508.
27. Ingham, J.L.; Keen, N.T.; Hymowitz, T. A new isoflavone phytoalexin from fungus-inoculated stems of Glycine wightii. Phytochemistry 1977, 16, 1943-1946.
28. Ingham, J.L. Flavonoid and isoflavonoid compounds from leaves of sainfoin (Onobrychis viciifolia). Z. Naturforsch. C 1978, 33, 146-148.
29. Ingham, J.L. Phytoalexins from hyacinth bean (Lablab niger). Z. Naturforsch. C 1977, 32, 1018-1020.
30. Hargreaves, J.A.; Mansfield, J.W.; Coxon, D.T. Identification of medicarpin as a phytoalexin in the broad bean plant (Vicia faba L.). Nature 1976, 262, 318-319.
31. Ingham, J.L. Phytolexin production by species of the genus Caragana. Z. Naturforsch. C 1979, 34, 293-295.
32. Gnanamanickam, S.S. Isolation of isoflavonoid phytoalexins from seeds of Phaseolus vulgaris. Experientia 1979, 35, 323.
33. Burden, R.S.; Bailey, J.A. Structure of the phytoalexin from soybean. Phytochemistry 1975, 14, 1389-1390.
34. Bonde, M.R.; Millar, R.L.; Ingham, J.L. Induction and identification of sativan and vestitol as two phytoalexins from Lotus cornicolatus. Phytochemistry 1973, 12, 2957-2959.
35. Lyon, F.M.; Wood, R.K.S. Production of phaseollin, coumestrol and related compounds in bean leaves inoculated with Pseudomonas spp. Physiol. Plant Pathol. 1975, 6, 117-124.
36. Mansfield, J.W.; Porter, A.E.A.; Smallman, R.V. Dihydrowyerone derivatives as components of the furanoacetylene phytoalexin response of tissues of Vicia faba. Phytochemistry 1980, 19, 1057-1061.
37. Hargreaves, J.A.; Mansfield, J.W.; Coxon, D.T. Conversion of wyerone to wyerol by Botrytis cinerea and B. fabae in vitro. Phytochemistry 1976, 15, 651-653.
38. Ingham, J.L. 3,5,4'-trihydroxystilbene as a phytoalexin from groundnuts (Arachis hypogea). Phytochemistry 1976, 15, 1791-1793.
39. Kuc, J. A biochemical study of the resistance of potato tuber to attack by various fungi. Phytopathology 1957, 47, 676-680.
40. Locci, R.; Kuc, J. Steroid glycoalkaloids as compounds produced by potato tuber slices under stress. Phytopathology 1967, 57, 1272-1273.
41. Tomiyama, K.; Sakuma, T.; Ishizaka, N.; Sato, N.; Takasugi, M.; Katsui, T. A new antifungal substance isolated from potato tuber tissue infected by pathogens. Phytopathology 1968, 58, 115-116.
42. Katsui, N.; Murai, A.; Takasugi, M.; Imaizumi, K.; Masamune, T. The structure of rishitin, a new anfifungal compound from diseased potato tubers. J. Chem. Soc. Chem. Comm. 1968, 43-44.
43. Katsui, N.; Matsunaga, A.; Masamune, T. The structure of lubimin, oxylubimin, antifungal metabolites from diseased potato tubers. Tetrahedron Lett. 1974, 15, 4483-4486.
44. 13C nuclear magnetic resonance of eremophilane derivatives having trans-vicinal methyl groups. Can. J. Chem. 1974, 52, 993-1005.
45. Reuveni, M.; Cohen, Y. Growth retardation and changes in phenolic compounds, with special reference to scopoletin, in mildewed and ethylene-treated tobacco plants. Physiol. Plant Pathol. 1978, 12, 179-189.
46. Cartwright, D.W.; Langcake, P.; Pryce, R.J.; Leworthy, D.P.; Ride, J.P. Isolation and characterization of two phytoalexins from rice as momilactones A and B. Phytochemistry 1981, 20, 535-537.
47. Kodama, O.; Miyakawa, J.; Akatsuka, T.; Kiyosawa, S. Sakuranetin, a flavanone phytoalexin from ultraviolet-irradiated rice leaves. Phytochemistry 1992, 31, 3807-3809.
48. Umemura, K.; Ogawa, N.; Shimura, M.; Koga, J.; Usami, H.; Kono, T. Possible role of phytocassane, rice phytoalexin, in disease resistance of rice against the blast fungus Magnaporthe grisae. Biosci. Biotechnol. Biochem. 2003, 67, 899-902.
49. Schmelz, E.A.; Kaplan, F.; Huffaker, A.; Dafoe, N.J.; Vaughan, M.M.; Ni, X.; Rocca, J.R.; Alborn, H.T.; Teal, P.E.A. Identity, regulation, and activity of inducible diterpenoid phytoalexins in maize. Proc. Natl. Acad. Sci. USA 2011, 108, 5455-5460.
50. Huffaker, A.; Kaplan, F.; Vaughan, M.M.; Dafoe, N.J.; Ni, X.; Rocca, J.R.; Alborn, H.T.; Teal, P.E.A.; Schmelz, E.A. Novel acidic sesquiterpenoids constitute a dominant class of pathogen-induced phytoalexins in maize. Plant Physiol. 2011, 156, 2082-2097.
51. Nicholson, F.; Kollipara, S.S.; Vincent, J.R.; Lyons, P.C.; Cadena-Gomez G. Phytoalexin synthesis by the sorghum mesocotyl in response to infection by pathogenic and nonpathogenic fungi. Proc. Natl. Acad. Sci. USA 1987, 84, 5520-5524.
52. Lo, S.C.; de Verdier, K.; Nicholson, R. Accumulation of 3-deoxyanthocyanidin phytoalexins and resistance to Colletotrichum sublineolum in sorghum. Physiol. Mol. Plant Pathol. 1999, 55, 263-273.
53. Ejike, C.E.C.C.; Gong, M.; Udenigwe, C.C. Phytoalexins from the Poaceae: Biosynthesis, function and prospects in food preservation. Food Res. Int. 2013, 52, 167-177.
54. Bell, A.A. Formation of gossypol in infected or chemically irritated tissues of Gossypium species. Phytopathology 1967, 57, 759-764.
55. Browne, L.M.; Conn, K.L.; Ayert, W.A.; Tewari, J.P. The camalexins: New phytoalexins produced in the leaves of Camelia sativa (Cruciferae). Tetrahedron 1991, 47, 3909-3914.
56. Langcake, P.; Pryce, R.J. The production of resveratrol by Vitis vinifera and other members of the Vitaceae as a response to infection or injury. Physiol. Plant Pathol. 1976, 9, 77-86.
57. Pérez-Clemente, R.M.; Vives, V.; Zandalinas, S.I.; Lopez-Climent, M.F.; Munoz, V.; Gomez-Cadenas, A. Biotechnological approaches to study plant responses to stress. BioMed. Res. Int. 2013, doi:10.1155/2013/654120.
58. Grosskinsky, D.K.; van der Graaff, E.; Roitsch, T. Phytoalexin transgenics in crop protection-Fairy tale with a happy end? Plant Sci. 2012, 195, 54-70.
59. Halls, C.; Yu, O. Potential for metabolic engineering of resveratrol biosynthesis. Trends Biotechnol. 2008, 26, 77-81.
60. Delaunois, B.; Cordelier, S.; Conreux, A.; Clément, C.; Jeandet, P. Molecular engineering of resveratrol in plants. Plant Biotechnol. J. 2009, 7, 2-12.
61. Donnez, D.; Jeandet, P.; Clément, C.; Courot, E. Bioproduction of resveratrol and stilbene derivatives by plant cells and microorganisms. Trends Biotechnol. 2009, 27, 706-713.
62. Jeandet, P.; Delaunois, B.; Conreux, A.; Donnez, D.; Nuzzo, V.; Cordelier, S.; Clément, C.; Courot, E. Biosynthesis, metabolism, molecular engineering and biological functions of stilbene phytoalexins in plants. BioFactors 2010, 36, 331-341.
63. Jeandet, P.; Delaunois, B.; Aziz, A.; Donnez, D.; Vasserot, Y.; Cordelier, S.; Courot, E. Metabolic engineering of yeast and plants for the production of the biologically active hydroxystilbene, resveratrol. J. Biomed. Biotechnol. 2012, doi:10.1155/2012/579089.
64. Jeandet, P., Vasserot, Y.; Chastang, T.; Courot, E. Engineering microbial cells for the biosynthesis of natural compounds of pharmaceutical significance. BioMed. Res. Int. 2013, doi:10.1155/2013/780145.
65. Hain, R.; Reif, H.J.; Krause, E.; Langebartels, R.; Kindl, H.; Vornam, B.; Wiese, W.; Schmelzer, E.; Schreier, P.; Stöcker, R.; Stenzel, K. Disease resistance results from foreign phytoalexin expression in a novel plant. Nature 1993, 361, 153-156.
66. Hipskind, J.D.; Paiva, N.L. Constitutive accumulation of a resveratrol glucoside in transgenic alfalfa increases resistance to Phoma medicaginis. Mol. Plant-Microbe Interact. 2000, 13, 551-562.
67. Coutos-Thévenot, P.; Poinssot, B.; Bonomelli, A.; Yean, H.; Breda, C.; Buffard, D.; Esnault, R.; Hain, R.; Boulay, M. In vitro tolerance to Botrytis cinerea of grapevine 41B rootstock in transgenic plants expressing the stilbene synthase Vst 1 gene under the control of a pathogen-inducible PR 10 promoter. J. Exp. Bot. 2001, 52, 901-910.
68. Stark-Lorenzen, P.; Nelke, B.; Hänbler, G.; Mühlbach, H.P.; Thomzik, J.E. Transfer of a grapevine stilbene synthase gene to rice (Oryza sativa L.). Plant Cell Rep. 1997, 16, 668-673.
69. Leckband, G.; Lörz, H. Transformation and expression of a stilbene synthase gene of Vitis vinifera L. in barley and wheat for increased fungal resistance. Theor. Appl. Genet. 1998, 96, 1004-1012.
70. Liang, H.; Zheng, J.; Shuange, J.I.A.; Wang, D.; Ouyang, J.; Li, J.; Li, L.; Tian, W.; Jia, X.; Duan, X.; Sheng, B.; Hain, R. A transgenic wheat with a stilbene synthase gene resistant to powdery mildew obtained by biolistic method. Chin. Sci. Bull. 2000, 45, 634-638.
71. Thomzik, J.E.; Stenzel, K.; Stöcker, R.; Schreier, P.H.; Hain, R.; Stahl, D.J. Synthesis of a grapevine phytoalexin in transgenic tomatoes (Lycopersicon esculentum Mill.) conditions resistance against Phytophthora infestans. Physiol. Mol. Plant Pathol. 1997, 51, 265-278.
72. Serazetdinova, L.; Oldach, K.; Lörz, H. Expression of transgenic stilbene synthases in wheat causes the accumulation of unknown stilbene derivatives with antifungal activity. J. Plant Physiol. 2005, 162, 985-1002.
73. Zhu, Y.J.; Agbayani, R.; Jazckson, M.C.; Tang, C.S.; Moore, P.M. Expression of the grapevine stilbene synthase gene VST1 in papaya provides increased resistance against diseaes caused by Phytophthora palmivora. Planta 2004, 12, 807-812.
74. Lim, J.D.; Yun, S.J.; Chung, I.M.; Yu, C.Y. Resveratrol synthase transgene expression and accumulation of resveratrol glycoside in Rehmannia glutinosa. Mol. Breed. 2005, 16, 219-233.
75. Liu, Z.Y.; Zhuang, C.X.; Sheng, S.J. Overexpression of a resveratrol synthase gene (PcRs) from Polygonum cuspidatum in transgenic Arabidopsis causes the accumulation of trans-piceid with antifungal activity. Plant Cell Rep. 2011, 30, 2027-2036.
76. Deavours, B.E.; Dixon, R.A. Metabolic engineering of isoflavonoid biosynthesis in alfalfa. Plant Physiol. 2005, 138, 2245-2259.
77. Kaimoyo, E.; VanEtten, H.D. Inactivation of pea genes by RNAi supports the involvement of two similar O-methyltransferases in the biosynthesis of (+)-pisatin and of chiral intermediates with a configuration opposite that found in (+)-pisatin. Phytochemistry 2008, 69, 76-87.
78. Giorcelli, A.; Sparvoli, F.; Mattivi, F.; Tava, A.; Balestrazzi, A.; Vrhovsek, U.; Calligari, P.; Bollini, R.; Confalonieri, M. Expression of the stilbene synthase (StSy) gene from grapevine in transgenic white poplar results in high accumulation of the antioxidant resveratrol glucosides. Transgenic Res. 2004, 13, 203-214.
79. Seppänen, S.K.; Syrjälä, L.; von Weissenberg, K.; Teeri, T.H.; Paajanen, L.; Pappinen, A. Antifungal activity of stilbenes in vitro bioassays and in transgenic Populus expressing a gene encoding pinosylvin synthase. Plant Cell Rep. 2004, 22, 584-593.
80. Kobayashi, S.; Ding, C.K.; Nakamura, Y.; Nakajima, I.; Matsumoto, R. Kiwifruits (Actinidia deliciosa) transformed with a Vitis stilbene synthase gene produce piceid (resveratrol-glucoside). Plant Cell Rep. 2000, 19, 904-910.
81. Fischer, R.; Budde, I.; Hain, R. Stilbene synthase gene expression causes changes in flower colour and male sterility in tobacco. Plant J. 1997, 11, 489-498.
82. Höfig, K.P.; Möller, R.; Donaldson, L.; Putterill, J.; Walter, C. Towards male sterility in Pinus radiata-A stilbene synthase approach to genetically engineer nuclear male sterility. Plant Biotechnol. J. 2006, 4, 333-343.
83. He, X.Z.; Dixon, R.A. Genetic manipulation of isoflavone 7-O-methyltransferase enhances biosynthesis of 4'-O-methylated isoflavonoid phytoalexins and disease resistance in alfalfa. Plant Cell 2000, 12, 1689-1702.
84. Blount, J.W.; Dixon, R.A.; Paiva, N.L. Stress responses in alfalfa (Medicago sativa L.) XVI. Antifungal activity of medicarpin and its biosynthetic precursors; implications for the genetic manipulation of stress metabolites. Physiol. Mol. Plant Pathol. 1993, 41, 333-349.
85. Wu, Q.; VanEtten, H.D. Introduction of plant and fungal genes into pea (Pisum sativum L.) hairy roots reduces their ability to produce pisatin and affects their response to a fungal pathogen. Mol. Plant-Microbe Interact. 2004, 17, 798-804.
86. Graham, T.L.; Graham, M.Y.; Subramanian, S.; Yu, O. RNAi silencing of genes for elicitation or biosynthesis of 5-deoxyisoflavonoids suppresses race-specific resistance and hypersensitive cell death in Phytophthora sojae infected tissues. Plant Physiol. 2007, 144, 728-740.
87. Ibraheem, F.; Gaffoor, I.; Chopra S. Flavonoid phytoalexin-dependent resistance to anthracnose leaf blight requires a functional yellow seed1 in Sorghum bicolor. Genetics 2010, 184, 915-926.
88. Shih, C.H.; Chu, I.K.; Yip, W.K.; Lo, C.S. Differential expression of two flavonoid 3'-hydroxylase cDNAs involved in biosynthesis of anthocyanin pigments and 3-deoxyanthocyanidin phytoalexins in sorghum. Plant Cell Physiol. 2006, 47, 1412-1419.
89. Sharma, M.; Chai, C.; Morohashi, K.; Grotewold, E.; Snook, M.E.; Chopra, S. Expression of flavonoid 3'-hydroxylase is controlled by P1, the regulator of 3-deoxyflavonoid biosynthesis in maize. BMC Plant Biol. 2012, 12, 196.
90. Boddu, J.; Svabek, C.; Ibraheem, F.; Jones, A.D.; Chopra, S. Characterization of a deletion allele of a sorghum Myb gene, yellow seed1 showing loss of 3-deoxyflavonoids. Plant Sci. 2005, 169, 542-552.
91. Boddu, J.; Jiang, C.; Sangar, V.; Olson, T.; Peterson, T.; Chopra, S. Comparative structural and functional characterization of sorghum and maize duplications containing orthologous myb transcription regulators of 3-deoxyflavonoid biosynthesis. Plant Mol. Biol. 2006, 60, 185-199.
92. Glazebrook, J.; Ausubel, F.M. Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc. Natl. Acad. Sci. USA 1994, 91, 8955-8959.
93. Glazebrook, J.; Zook, M.; Mert, F.; Kagan, I.; Rogers, E.E.; Crute, I.; Holub, E.; Hammerschmidt, R.; Ausubel, F.M. Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics 1997, 146, 381-392.
94. Reuber, T.L.; Plotnikova, J.M.; Dewdnev, J.; Rogers, E.E.; Wood, W.; Ausubel, F.M. Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. Plant J. 1998, 16, 473-485.
95. Ahl-Goy, P.; Signer, H.; Reist, R.; Aichholz, R.; Blum, B.; Schmidt, E.; Kessmann, H. Accumulation of scopoletin is associated with the high disease resistance of the hybrid Nicotiana tabacum × Nicotiana debneyi. Planta 1993, 191, 200-206.
96. Gnonlonfin, G.J.B.; Sanni, A.; Brimer, L. Scopoletin-A coumarin phytoalexin with medicinal properties. Crit. Rev. Plant Sci. 2012, 31, 47-56.
97. Li, Y.; Baldauf, S.; Lim, E.K.; Bowles, J.D. Phylogenetic analysis of the UDP-glycosyltransferase multigene family of Arabidopsis thaliana. J. Biol. Chem. 2001, 276, 4338-4343.
98. Chong, J.; Baltz, R.; Schmitt, C.; Beffa, R.; Fritig, B.; Saindrenan, P. Downregulation of a pathogen-responsive tobacco UDP-Glc:phenylpropanoid glucosyltransferase reduces scopoletin glucoside accumulation, enhances oxidative stress, and weakens virus resistance. Plant Cell 2002, 14, 1093-1107.
99. Gachon, C.; Baltz, R.; Saindrenan, P. Over-expression of a scopoletin glucosyltransferase in Nicotiana tabacum leads to precocious lesion formation during the hypersensitive response to tobacco mosaic virus but does not affect virus resistance. Plant Mol. Biol. 2004, 54, 137-146.
100. Grosskinsky, D.K.; Naseem, M.; Abdelmoshem, U.A.; Plickert, N.; Engelke, T.; Griebel, T.; Zeier, J.; Novak, O.; Strand, M.; Pfeifhofer, H., et al. Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling. Plant Physiol. 2011, 157, 815-830.
101. Mauch-Mani, B.; Mauch, F. The role of abscissic acid in plant-pathogen interactions. Curr. Opin. Plant Biol. 2005, 8, 409-414.
102. Jones, J.D.; Dangles, J.L. The plant immune system. Nature 2006, 444, 323-329.
103. Robert-Seilaniantz, A.; Navarro, L.; Bari, R.; Jones, J.D. Pathological hormone imbalances. Curr. Opin. Plant Biol. 2007, 10, 372-379.
104. Asselbergh, B.; de Vleesschauwer, D.; Höfte, M. Global switches and fine-tuning-ABA modulates plant pathogen defense. Mol. Plant-Microbe Interact. 2008, 21, 709-719.
105. Lopez, M.A.; Bannenberg, G.; Castresana, C. Controlling hormone signaling is a plant and pathogen challenge for growth and survival. Curr. Opin. Plant Biol. 2008, 11, 420-427.
106. Spoel, S.H.; Dong, X. Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 2008, 3, 348-351.
107. Bari, R.; Jones J.D. Role of plant hormones in plant defence responses. Plant Mol. Biol. 2009, 69, 473-488.
108. Verhage, A.; van Wees, S.C.M.; Pieterse, C.M.J. Plant immunity: It's the hormones talking, but what do they say? Plant Physiol. 2010, 154, 536-540.
109. Erb, M.; Meldau, S.; Howe, G.A. Role of phytohormones in insect-specific plant reactions. Trends Plant Sci. 2012, 17, 250-259.
110. Navarro, L.; Dunoyer, P.; Jay, F.; Arnold, B.; Dharmasiri, N.; Estelle, M.; Voinnet, O.; Jones, J.D.G. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 2006, 312, 436-439.
111. Domingo, C.; Andrès, F.; Tharreau, D.; Iglesias, D.J.; Talon, M. Constitutive expression of OsGH3.1 reduces auxin content and enhances defense responses and resistance to a fungal pathogen in rice. Mol. Plant-Microbe Interact. 2009, 22, 201-210.
112. Mayda, E.; Marqués, M.C.; Conejero, V.; Vera, P. Expression of a pathogen-induced gene can be mimicked by auxin insensitivity. Mol. Plant-Microbe Interact. 2000, 13, 23-31.
113. Padmanabhan, M.S.; Goregaoker, S.P.; Golem, S.; Shiferaw, H.; Culver, J.N. Interaction of the tobacco mosaic virus replicase protein with the Aux/IAA protein PAP1/IAA26 is associated with disease development. J. Virol. 2005, 79, 2549-2558.
114. Padmanabhan, M.S.; Shiferaw, H.; Culver, J.N. The tobacco mosaic virus replicase protein disrupts the localization and function of interacting Aux/IAA proteins. Mol. Plant-Microbe Interact. 2006, 19, 864-873.
115. Ding, X.; Cao, Y.; Huang, L.; Zhao, J.; Xu, C.; Li, X.; Wang, S. Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate-and jasmonate-independent basal immunity in rice. Plant Cell 2008, 20, 228-240.
116. Iriti, M.; Faro, F. Chemical diversity and defence metabolism: How plant cope with pathogens and ozone pollution. Int. J. Mol. Sci. 2009, 10, 3371-3399.
117. Ristaino, J.B.; Duniway, J.M. Effect of preinoculation and postinoculation water-stress on the severity of Phytophthora root-rot in processing tomatoes. Plant Dis. 1989, 73, 349-352.
118. Audenaert, K.; de Meyer, G.B.; Höfte, M.M. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol. 2002, 128, 491-501.
119. Asselbergh, B.; Achuo, A.E.; Höfte, M.; van Breusegem, F. Abscisic acid deficiency leads to rapid activation of tomato defence responses upon infection with Erwinia chrysanthemi. Mol. Plant Pathol. 2008, 9, 11-24.
120. Balazs, E.; Gaborjanyi, R.; Kiraly, Z. Leaf senescence and increased virus susceptibility in tobacco: The effect of abscisic acid. Physiol. Mol. Plant Pathol. 1973, 3, 341-346.
121. Rezzonico, E.; Flury, N.; Meins, F., Jr.; Beffa, R. transcriptional down-regulation by abscisic acid of pathogenesis-related beta-1,3-glucanase genes in tobacco cell cultures. Plant Physiol. 1998, 117, 585-592.
122. Goosens, J.F.V.; Vendrig, J.C. Effects of abscissic acid, cytokinins, and light on isoflavonoid phytoalexin accumulation in Phaseolus vulgaris. Planta 1982, 154, 441-446.
123. Ward, E.W.; Cahill, D.M.; Bhattacharyya, M.K. Abscisic acid suppression of phenylalanine ammonia-lyase activity and mRNA, and resistance of soybeans to Phytophthora megasperma f.s.p. glycinea. Plant Physiol. 1989, 91, 23-27.
124. Mohr, P.; Cahill, D.M. Relative roles of glyceollin, lignin and the hypersensitive response and the influence of ABA in compatible and incompatible interactions of soybeans with Phytophthora sojae. Physiol. Mol. Plant Pathol. 2001, 58, 31-41.
125. Henfling, J.W.D.M.; Bostock, R.M.; Kuc, J. Effect of abscisic acid on rishitin and lubimin accumulation and resistance to Phytophthora infestans and Cladosporium cucumerinum in potato tuber tissue slices. Phytopathology 1980, 70, 1074-1078.
126. Mialoundama, A.S.; Heintz, D.; Debayle, D.; Rahier, A.; Camara, B.; Bouvier, F. Abscisic acid negatively regulates elicitor-induced synthesis of capsidiol in wild tobacco. Plant Physiol. 2009, 150, 1556-1566.
127. Thomas, S.G.; Phillips, A.L.; Hedden, P. Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc. Natl. Acad. Sci. USA 1999, 96, 4698-4703.
128. Yang, D.L.; Li, Q.; Deng, Y.W.; Lou, Y.G.; Wang, M.Y.; Zhou, G.X.; Zhang, Y.Y.; He, Z.H. Altered disease development in the eui mutants and Eui overexpressors indicates that gibberellins negatively regulate rice basal disease resistance. Mol. Plant 2008, 1, 528-537.
129. Sakakibara, H. Cytokinins: Activity, biosynthesis, and translocation. Annu. Rev. Plant Biol. 2006, 57, 431-449.
130. Sano, H.; Seo, S.; Koizumi, N.; Niki, T.; Iwamura, H.; Ohashi, Y. Regulation by cytokinins of endogenous levels of jasmonic and salicylic acids in mechanically wounded tobacco plants. Plant Cell Physiol. 1996, 37, 762-769.
131. Pogany, M.; Koehl, J.; Heiser, I.; Elstner, E.; Barna, B. Juvenility of tobacco induced by cytokinin gene introduction decreases susceptibility to Tobacco necrosis virus and confers tolerance to oxidative stress. Physiol. Mol. Plant Pathol. 2004, 65, 39-47.
132. Barna, B.; Smigocki, A.C.; Baker, J.C. Transgenic production of cytokinin suppresses bacterially induced hypersensitive response symptoms and increases antioxidative enzyme levels in Nicotiana spp. Phytopathology 2008, 98, 1242-1247.
133. Choi, J.; Huh, S.U.; Kojima, M.; Sakakibara, H.; Paek, K.H.; Hwang, I. The cytokinin-activated transcription factor A RR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis. Dev. Cell 2010, 19, 284-295.
134. Boller, T.; Felix, G. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 2009, 60, 379-406.
135. Dodds, P.N.; Rathjen, J.P. Plant mmunity: Towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 2010, 11, 539-548.
136. Newmann, M.A.; Sundelin, T.; Nielsen, J.T.; Erbs, G. MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front. Plant Sci. 2013, 4, 139.
137. Pitzschke, A.; Schikora, A.; Hirt, H. MAPK cascade signaling networks in plant defence. Curr. Opin. Plant Biol. 2009, 12, 421-426.
138. Garcia-Brugger, A.; Lamotte, O.; Vandelle, E.; Bourque, S.; Lecourieux, D.; Poinssot, B.; Wendehenne, D.; Pugin, A. Early signaling events induced by elicitors of plant defenses. Mol. Plant-Microbe Interact. 2006, 19, 711-724.
139. Zhao, J.; Last, R.L. Coordinate regulation of the tryptophan biosynthetic pathway and indolic phytoalexin accumulation in Arabidopsis. Plant Cell 1996, 8, 2235-2244.
140. Su, T.; Xu, J.; Li, Y.; Lei, L.; Zhao, L.; Yang, H.; Feng, J.; Liu, G.; Ren, D. Glutathione-indole-3-acetonitrile is required for camalexin biosynthesis in Arabidopsis thaliana. Plant Cell 2011, 23, 364-380.
141. Kim, J.A.; Cho, K.; Singh, R.; Jung, Y.H.; Jeong, S.H.; Kim, S.H.; Lee, J.E.; Cho, Y.S.; Agrawal, G.K.; Rakwal, R., et al. Rice OsACDR1 (Oryza sativa accelerated cell death and resistance 1) is a potential positive regulator of fungal disease resistance. Mol. Cells 2009, 28, 431-439.
142. Grant, M.; Lamb, C. Systemic immunity. Curr. Opin. Plant Biol. 2006, 9, 414-420.
143. Cao, H.; Li, X.; Dong, X. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc. Natl. Acad. Sci. USA 1998, 95, 6531-6536.
144. Quilis, J.; Penas, G.; Messeguer, J.; Brugidou, C.; San Segundo, B. The Arabidopsis AtNPR1 inversely modulates defense responses against fungal, bacterial, or viral pathogens while conferring hypersensitivity to abiotic stresses in transgenic rice. Mol. Plant-Microbe Interact. 2008, 21, 1215-1231.
145. Lin, W.C.; Lu, C.F.; Wu, J.W.; Cheng, M.L.; Lin, Y.M.; Yang, N.S.; Black, L.; Green, S.K.; Wang, J.F.; Cheng, C.P. Transgenic tomato plants expressing the Arabidopsis NPR1 gene display enhanced resistance to a spectrum of fungal and bacterial diseases. Transgenic Res. 2004, 13, 567-581.
146. Makandar, R.; Essig, J.S.; Schapaugh, M.A.; Trick, H.N.; Shah, J. Genetically engineered resistance to Fusarium head blight in wheat by expression of Arabidopsis NPR1. Mol. Plant-Microbe Interact. 2006, 19, 123-129.
147. Wally, O.; Jayaraj, J.; Punja, Z.K. Broad-spectrum disease resistance to necrotrophic and biotrophic pathogens in trnsgnic carrots (Daucus carota L.) expressing an Arabidopsis NPR1 gene. Planta 2009, 231, 131-141.
148. Parkhi, V.; Kumar, V.; Campbell, L.M.; Bell, A.A.; Shah, J.; Rathore, K.S. Resistance against various fungal pathogens and reniform nematode in transgenic cotton plants expressing Arabidopsis NRP1. Transgenic Res. 2010, 19, 959-975.
149. Berken, A. ROPs in the spotlight of plant signal transduction. Cell. Mol. Life Sci. 2006, 63, 2446-2459.
150. Ono, E.; Wong, H.L.; Kawasaki, T.; Hasegawa, M.; Kodama, O.; Shimamoto, K. Essential role of the small GTPase Rac in disease resistance of rice. Proc. Natl. Acad. Sci. USA 2001, 98, 759-764.
151. Kawano, Y.; Akamatsu, A.; Hayashi, K.; Housen, Y.; Okuda, J.; Yao, A.; Nakashima, A.; Takahashi, H.; Yoshida, H.; Wong, H.L., et al. Activation of a Rac GTPase by the NLR family disease resistance protein pit plays a critical role in rice innate immunity. Cell Host Microbe 2010, 7, 362-375.
152. Chen, L.; Shiotani, K.; Togashi, T.; Miki, D.; Aoyama, M.; Wong, H.L.; Kawasaki, T.; Shimamoto, K. Analysis of the Rac/Rop small GTPase family in rice: Expression, subcellular localization and role in disease resistance. Plant Cell Physiol. 2010, 51, 85-95.
153. Sadawa, K.; Hasegawa, M.; Tokuda, L.; Kameyama, J.; Kodama, O.; Kohchi, T.; Yoshida, K.; Shinmyo, A. Enhanced resistance to blast fungus and bacterial blight in transgenic rice constitutively expressing OsSBP, a rice homologue of mamalian selenium-binding proteins. Biosci. Biotechnol. Biochem. 2004, 68, 873-880.
154. Flemetakis, E.; Agalou, A.; Kavroulakis, N.; Dimou, M.; Martsikovskaya, A.; Slater, A.; Spaink, H.P.; Roussis, A.; Katinakis, P. Lotus japonicus gene Ljsbp is highly conserved among plants and animals and encodes a homologue to the mamalian selenium-binding proteins. Mol. Plant-Microbe Interact. 2002, 15, 313-322.
155. Sawada, K.; Tokuda, L.; Shinmyo, A. Characterization of the rice blast fungal elicitor-responsive gene OsSBP encoding a homolog to the mamalian selenium-binding proteins. Plant Biotechnol. 2003, 20, 179-183.
156. Dodd, A.N.; Kudla, J.; Sanders, D. The language of calcium signalling. Annu. Rev. Plant Biol. 2010, 61, 593-620.
157. Reddy, A.S.; Ali G.S.; Celesnik H.; Day I.S. Coping with stresses: Roles of calcium-and calcium/calmodulin-regulated gene expression. Plant Cell 2011, 23, 2010-2032.
158. Romeis, T.; Ludwig, A.; Martin, R.; Jones, J.D.G. Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J. 2001, 20, 5556-5567.
159. Luan, S. The CBL-CIPK network in plant calcium signaling. Trends Plant Sci. 2009, 14, 37-42.
160. Kurusu, T.; Hamada, J.; Nokajima, H.; Kitagawa, Y.; Kiyoduka, M.; Takahashi, A.; Hanamata, S.; Ohno, R.; Hayashi, T.; Okada, K., et al. Regulation of microbe-associated molecular pattern-induced hypersensitive cell death, phytoalexin production, and defense gene expression by calcineurin B-like protein-interacting protein kinases, OsCIPK14/15, in rice cultured cells. Plant Physiol. 2010, 153, 678-692.
161. Okada, K. The biosynthesis of isoprenoids and the mechanisms regulating it in plants. Biosci. Biotechnol. Biochem. 2011, 75, 1219-1225.
162. Rauhut, T.; Luberacki, B.; Seitz, H.U.; Glawischnig, E. Inducible expression of a Nep1-like protein serves as a model trigger system of camalexin biosynthesis. Phytochemistry 2009, 70, 185-189.
163. Pemberton, C.L.; Salmond, G.P.C. The Nep1-like proteins-A growing family of microbial elicitors of plant necrosis. Mol. Plant Pathol. 2004, 5, 353-359.
164. Qutob, D.; Kemmerling, B.; Brunner, F.; Küfner, L.; Engelhardt, S.; Gust, A.A.; Luberacki, B.; Seitz, H.U.; Stahl, D.; Rauhut, T., et al. Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell 2006, 18, 3721-3744.
165. Mori, M.; Tomita, C.; Sugimoto, K.; Hasegawa, M.; Hayashi, N.; Dubouzet, J.G.; Ochiai, H.; Sekimoto, H.; Hirochika, H.; Kikuchi, S. Isolation and molecular characterization of a Spotted leaf 18 mutant by modified activation-tagging in rice. Plant Mol. Biol. 2007, 63, 847-860.
166. Kachroo, A.; Lapchyk, L.; Fukushige, H.; Hildebrand, D.; Klessig, D.; Kachroo, P. Plastidial fatty acid signaling modulates salicylic acid-and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. Plant Cell 2003, 15, 2952-2965.
167. Kachroo, A.; Venugopal, S.C.; Lapchyk, L.; Falcone, D.; Hildebrand, D.; Kachroo, P. Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proc. Natl. Acad. Sci. USA 2004, 101, 5152-5157.
168. Matthews, D.; Jones, H.; Gans, P.; Coates, S.; Smith, L.M.J. Toxic secondary metabolite production in genetically modified potatoes in response to stress. J. Agric. Food Chem. 2005, 53, 7766-7776.
169. Benedict, C.R.; Lu, J.L.; Pettigrew, D.W.; Liu, J.; Stipanovic, R.D.; Williams, H.J. The cyclization of farnesyl diphosphate and nerolidyl diphosphate by a purified recombinant δ-cadinene synthase. Plant Physiol. 2001, 125, 1754-1765.
170. Martin, G.S.; Liu, J.; Benedict, C.R.; Stipanovic, R.D.; Magill, W.M. Reduced levels of cadinane sesquiterpenoids in cotton plants expressing antisense (+)-δ-cadinene synthase. Phytochemistry 2003, 62, 31-38.
171. Chen, X.Y.; Chen, Y.; Heinstein, P.; Davisson, V.J. Cloning, expression, and characterization of (+)-δ-cadinene synthase: A catalyst for cotton phytoalexin biosynthesis. Arch. Biochem. Biophys. 1995, 324, 255-266.
172. Chen, X.Y.; Wang, M.; Chen, Y.; Davisson, V.J.; Heinstein, P. Cloning and heterologous expression, and characterization of a second (+)-δ-cadinene synthase from Gossypium arboreum. J. Nat. Prod. 1996, 59, 944-951.
173. Kalani, R.; Gamboa, D.A.; Calhoun, M.C.; Haq, A.U.; Bailey, C.A. Relative toxicity of cottonseed gossypol enantiomers in broilers. Open Toxicol. J. 2010, 4, 26-31.
174. Townsend, B.J.; Poole, A.; Blake, C.J.; Llewellyn, D.J. Antisense suppression of a (+)-δ-cadinene synthase gene in cotton prevents the induction of this defense response gene during blight infection but not its constitutive expression. Plant Physiol. 2005, 138, 516-528.
175. Benedict, C.R.; Martin, G.S.; Liu, J.; Puckhaber, L.; Magill, C.W. Terpenoid aldehyde formation and lysigenous gland storage sites in cotton: Variant with mature glands but suppressed levels of terpenoid aldehydes. Phytochemistry 2004, 65, 1351-1359.
176. Sunilkumar, G.; Campbell, L.M.; Pukhaber, L.; Stipanovic, R.D.; Rathore, K.S. Engineering cottonseed for use in human nutrition by tissue-specific reduction of toxic gossypol. Proc. Natl Acad. Sci. USA 2006, 103, 18054-18059.
177. Sunilkumar, G.; Connell, J.P.; Smith, C.W.; Reddy, A.S.; Rathore, K.S. Cotton α-globulin promoter: Isolation and functional characterization in transgenic cotton, Arabidospsis, and tobacco. Transgenic Res. 2002, 11, 347-359.
178. Rathore, K.S.; Sunilkumar, G.; Campbell, L.M. Cotton plant with seed specific reduction in gossypol. US Patent N° 20070199098, 16 February 2007.