Transcriptome analysis of tobacco BY-2 cells elicited by cryptogein reveals new potential actors of calcium-dependent and calcium-independent plant defense pathways

Cell Calcium

Volumn 51, Issue 2, 2012, Pages 117-130

  Amelot, Nicolas ^a,b   Dorlhac de Borne, François ^c   San Clemente, Hélène ^a,b   Mazars, Christian ^a,b   Grima Pettenati, Jacqueline ^a,b   Brière, Christian ^a,b  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b CNRS   (France)

^c Altadis Institut du Tabac   (France)

Author keywords

Calcium signaling; Cryptogein; Nicotiana tabacum (tobacco BY 2); Transcription regulation

Indexed keywords

CALCIUM ION; CRYPTOGEIN; HEAT SHOCK PROTEIN; LANTHANUM CHLORIDE; OXYLIPIN; PEPTIDE DERIVATIVE; PHENOL DERIVATIVE; PHENYLPROPANOID; TRANSCRIPTION FACTOR; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; CELL WALL; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; MICROARRAY ANALYSIS; NONHUMAN; PLANT CELL; PLANT DEFENSE; PLANT GENE; PLANT GENOME; PLANT METABOLISM; PLANT STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TOBACCO; TRANSCRIPTION REGULATION; TRANSCRIPTOME ANALYSIS; TRANSCRIPTOMICS;

NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; PHYTOPHTHORA CRYPTOGEA;

EID: 84856953669     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2011.11.010     Document Type: Article

References (104)

1. Scheel D. Resistance response physiology and signal transduction. Curr. Opin. Plant Biol. 1998, 1(4):305-310.
2. Grant M., Lamb C. Systemic immunity. Curr. Opin. Plant Biol. 2006, 9(4):414-420.
3. Lam E., Kato N., Lawton M. Programmed cell death, mitochondria and the plant hypersensitive response. Nature 2001, 411(6839):848-853.
4. Lam E. Controlled cell death, plant survival and development. Nat. Rev. Mol. Cell. Biol. 2004, 5(4):305-315.
5. Greenberg J.T., Yao N. The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol. 2004, 6(3):201-211.
6. Hatsugai N., Kuroyanagi M., Yamada K., Meshi T., Tsuda S., Kondo M., Nishimura M., Hara-Nishimura I. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 2004, 305(5685):855-858.
7. Lecourieux D., Mazars C., Pauly N., Ranjeva R., Pugin A. Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 2002, 14(10):2627-2641.
8. Wendehenne D., Durner J., Klessig D.F. Nitric oxide: a new player in plant signalling and defence responses. Curr. Opin. Plant Biol. 2004, 7(4):449-455.
9. Nürnberger T., Brunner F., Kemmerling B., Piater L. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 2004, 198:249-266.
10. Ponchet M., Panabières F., Milat M.L., Mikes V., Montillet J.L., Suty L., Triantaphylides C., Tirilly Y., Blein J.P. Are elicitins cryptograms in plant-oomycete communications. Cell. Mol. Life Sci. 1999, 56(11-12):1020-1047.
11. Ricci P., Bonnet P., Huet J.C., Sallantin M., Beauvais-Cante F., Bruneteau M., Billard V., Michel G., Pernollet J.C. Structure and activity of proteins from pathogenic fungi Phytophtora eliciting necrosis and acquired resistance in tobacco. Eur. J. Biochem. 1989, 183:555-563.
12. Keller H., Blein J.P., Bonnet P., Ricci P. Physiological and molecular characteristics of elicitin-induced systemic acquired resistance in tobacco. Plant Physiol. 1996, 110(2):365-376.
13. Bourque S., Binet M.N., Ponchet M., Pugin A., Lebrun-Garcia A. Characterization of the cryptogein binding sites on plant plasma membranes. J. Biol. Chem. 1999, 274(49):34699-34705.
14. Blein J.P., Milat M.L., Ricci P. Responses of cultured tobacco cells to cryptogein, a proteinaceous elicitor from Phytophthora cryptogea: possible plasmalemma involvement. Plant Physiol. 1991, 95(2):486-491.
15. Garcia-Brügger 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.
16. Simon-Plas F., Elmayan T., Blein J.P. The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. Plant J. 2002, 31(2):137-147.
17. Simon-Plas F., Rusterucci C., Milat M.L., Humbert C., Montillet J.L., Blein J.P. Active oxygen species production in tobacco cells elicited by cryptogein. Plant Cell Environ. 1997, 20:1573-1579.
18. Tavernier E., Wendehenne D., Blein J.P., Pugin A. Involvement of free calcium in action of cryptogein, a proteinaceous elicitor of hypersensitive reaction in tobacco cells. Plant Physiol. 1995, 109(3):1025-1031.
19. Wendehenne D., Lamotte O., Frachisse J.M., Barbier-Brygoo H., Pugin A. Nitrate efflux is an essential component of the cryptogein signaling pathway leading to defense responses and hypersensitive cell death in tobacco. Plant Cell 2002, 14:1937-1951.
20. Cheong Y.H., Chang H.S., Gupta R., Wang X., Zhu T., Luan S. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 2002, 129(2):661-677.
21. Moscatiello R., Mariani P., Sanders D., Maathuis F.J. Transcriptional analysis of calcium-dependent and calcium-independent signalling pathways induced by oligogalacturonides. J. Exp. Bot. 2006, 57(11):2847-2865.
22. Navarro L., Zipfel C., Rowland O., Keller I., Robatzek S., Boller T., Jones J.D. The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol. 2004, 135(2):1113-1128.
23. Galon Y., Finkler A., Fromm H. Calcium-regulated transcription in plants. Mol. Plant 2010, 3:653-669.
24. 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.
25. Lecourieux D., Ranjeva R., Pugin A. Calcium in plant defence-signalling pathways. New Phytol. 2006, 171(2):249-269.
26. Pauly N., Knight M.R., Thuleau P., van der Luit A.H., Moreau M., Trewavas A.J., Ranjeva R., Mazars C. Cell signalling: control of free calcium in plant cell nuclei. Nature 2000, 405:754-755.
27. Xiong T.C., Bourque S., Lecourieux D., Amelot N., Grat S., Brière C., Mazars C., Pugin A., Rangeva R. Calcium signaling in plant cell organelles delimited by a double membrane. Biochim. Biophys. Acta 2006, 1763:1209-1215.
28. Xiong T.C., Jauneau A., Ranjeva R., Mazars C. Isolated plant nuclei as mechanical and thermal sensors involved in calcium signalling. Plant J. 2004, 40:12-21.
29. Takahashi K., Isobe M., Knight M.R., Trewavas A.J., Muto S. Hypoosmotic shock induces increases in cytosolic Ca2+ in tobacco suspension-culture cells. Plant Physiol. 1997, 113:587-594.
30. Pauly N., Knight M.R., Thuleau P., Graziana A., Muto S., Ranjeva R., Mazars C. The nucleus together with the cytosol generates patterns of specific cellular calcium signatures in tobacco suspension culture cells. Cell Calcium 2001, 30:413-421.
31. Bonnet P., Bourdon E., Ponchet M., Blein J.P., Ricci P. Acquired resistance triggered by elicitins in tobacco and other plants. Eur. J. Plant Pathol. 1996, 102:181-192.
32. Li C., Wong W.H. Model-based analysis of oligonucleotides arrays: model validation, design issues and standard error application. Genome Biol. 2001, 2(8). (research 0032.1-0032.11).
33. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 1995, 57:289-300.
34. Gentleman R., Carey V.J., Bates D.M., Bolstad B., Dettling M., Dudoit S., Ellis B., Gautier L., Ge Y., et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004, 5(R80).
35. Smyth G.K. Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions using R and Bioconductor 2005, 397-420. Springer, New York. R. Gentleman, V. Carey, S. Dudoit, R. Irizarry, W. Huber (Eds.).
36. Gautier L., Cope L., Bolstad B.M., Irizarry R.A. Affy-analysis of affymetrix GeneChip data at the probe level. Bioinformatics 2004, 20(3):307-315.
37. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
38. Amelot N., Carrouché A., Danoun S., Bourque S.H.J., Pugin A., Ranjeva R., Grima-Pettenati J., Mazars C., Brière C. Cryptogein, a fungal elicitor, remodels the phenylpropanoid metabolism of tobacco cell suspension cultures in a calcium-dependent manner. Plant Cell Environ. 2011, 34:149-161.
39. Lecourieux-Ouaked F., Pugin A., Lebrun-Garcia A. Phosphoproteins involved in the signal transduction of cryptogein, an elicitor of defense reactions in tobacco. Mol. Plant Microbe Interact. 2000, 13(8):821-829.
40. Rowland O., Ludwig A.A., Merrick C.J., Baillieul F., Tracy F.E., Durrant W.E., Fritz-Laylin L., Nekrasov V., Sjölander K., Yoshioka H., Jones J.D. Functional analysis of Avr9/Cf-9 rapidly elicited genes identifies a protein kinase, ACIK1, that is essential for full Cf-9-dependent disease resistance in tomato. Plant Cell 2005, 17(1):295-310.
41. Maurel C., Verdoucq L., Luu D.T., Santoni V. Plant aquaporins: membrane channels with multiple integrated functions. Annu. Rev. Plant Biol. 2008, 59:595-624.
42. Tyerman S.D., Niemietz C.M., Bramley H. Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ. 2002, 25(2):173-194.
43. Werner M., Uehlein N., Proksch P., Kaldenhoff R. Characterization of two tomato aquaporins and expression during the incompatible interaction of tomato with the plant parasite Cuscuta reflexa. Planta 2001, 213(4):550-555.
44. Dowd C., Wilson I.W., McFadden H. Gene expression profile changes in cotton root and hypocotyl tissues in response to infection with Fusarium oxysporum f. sp. vasinfectum. Mol. Plant Microbe Interact. 2004, 17(6):654-667.
45. Balague C., Lin B., Alcon C., Flottes G., Malmstrom S., Kohler C., Neuhaus G., Pelletier G., Gaymard F., Roby D. HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 2003, 15:365-379.
46. Mori I.C., Murata Y., Yang Y., Munemasa S., Wang Y.F., Andreoli S., Tiriac H., Alonso J.M., Harper J.F., Ecker J.R., Kwak J.M., Schroeder J.I. CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLoS Biol. 2006, 4:1749-1762.
47. Xu J., Tian Y.S., Peng R.H., Xiong A.S., Zhu B., Jin X.F., Gao F., Fu X.Y., Hou X.L., Yao Q.H. AtCPK6, a functionally redundant and positive regulator involved in salt/drought stress tolerance in Arabidopsis. Planta 2010, 231(6):1251-1260.
48. Oecking C., Jaspert N. Plant 14-3-3 proteins catch up with their mammalian orthologs. Curr. Opin. Plant Biol. 2009, 12(6):760-765.
49. Roberts M.R. 14-3-3 proteins find new partners in plant cell signalling. Trends Plant Sci. 2003, 8(5):218-223.
50. Konagaya K.-i., Matsushita Y., Kasahara M., Nyunoya H. Members of 14-3-3 protein isoforms interacting with the resistance gene product N and the elicitor of Tobacco mosaic virus. J. Gen. Plant Pathol. 2004, 70:221-231.
51. Elmayan T., Fromentin J., Riondet C., Alcaraz G., Blein J.P., Simon-Plas F. Regulation of reactive oxygen species production by a 14-3-3 protein in elicited tobacco cells. Plant Cell Environ. 2007, 30(6):722-732.
52. Gardner H.W. Recent investigations into the lipoxygenase pathway of plants. Biochim. Biophys. Acta 1991, 1084(3):221-239.
53. Andrews D.L., Beames B., Summers M.D., Park W.D. Characterization of the lipid acyl hydrolase activity of the major potato (Solanum tuberosum) tuber protein, patatin, by cloning and abundant expression in a baculovirus vector. Biochem. J. 1988, 252(1):199-206.
54. Browse J. The power of mutants for investigating jasmonate biosynthesis and signaling. Phytochemistry 2009, 70(13-14):1539-1546.
55. Gfeller A., Liechti R., Farmer E.E. Arabidopsis jasmonate signaling pathway. Sci. Signal 2010, 3(16 February (109)). p. cm4.
56. Wang C., Zien C.A., Afitlhile M., Welti R., Hildebrand D.F., Wang X. Involvement of phospholipase D in wound-induced accumulation of jasmonic acid in arabidopsis. Plant Cell 2000, 12(11):2237-2246.
57. Wang X. Lipid signaling. Curr. Opin. Plant Biol. 2004, 7(3):329-336.
58. Weber H., Chételat A., Caldelari D., Farmer E.E. Divinyl ether fatty acid synthesis in late blight-diseased potato leaves. Plant Cell 1999, 11(3):485-494.
59. Gullner G., Künstler A., Király L., Pogány M., Tóbiás I. Up-regulated expression of lipoxygenase and divinyl ether synthase genes in pepper leaves inoculated with Tobamoviruses. Physiol. Mol. Plant Pathol. 2010, 74:387-393.
60. Fammartino A., Verdaguer B., Fournier J., Tamietti G., Carbonne F., Esquerre-Tugaye M.T., Cardinale F. Coordinated transcriptional regulation of the divinyl ether biosynthetic genes in tobacco by signal molecules related to defense. Plant Physiol. Biochem. 2010, 48:225-231.
61. Eulgem T., Somssich I.E. Networks of WRKY transcription factors in defence signaling. Curr. Opin. Plant Biol. 2007, 10(4):366-371.
62. Jensen M.K., Hagedorn P.H., de T.-Z.M., Grant M.R., Rung J.H., Collinge D.B., Lyngkjaer M.F. Transcriptional regulation by an NAC (NAM-ATAF1,2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. Plant J. 2008, 56(6):867-880.
63. Libault M., Wan J.R., Czechowski T., Udvardi M., Stacey G. Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol. Plant Microbe Interact. 2007, 20:900-911.
64. Shinya T., Galis I., Narisawa T., Sasaki M., Fukuda H., Matsuaka H., Saito M., Matsuoka K. Comprehensive analysis of glucan elicitor-regulated gene expression in tobacco BY-2 cells reveals a novel MYB transcription factor involved in the phenylpropanoid metabolism. Plant Cell Physiol. 2007, 48:1404-1413.
65. Maeda K., Kimura S., Demura T., Takeda J., Ozeki Y. DcMYB1 acts as a transcriptional activator of the carrot phenylalanine ammonia-lyase gene (DcPAL1) in response to elicitor treatment, UV-B irradiation and the dilution effect. Plant Mol. Biol. 2005, 59(5):739-752.
66. Hui D., Iqbal J., Lehmann K., Gase K., Saluz H.P., Baldwin I.T. Molecular interactions between the specialist herbivore Manduca sexta (lepidoptera, sphingidae) and its natural host Nicotiana attenuata: V. microarray analysis and further characterization of large-scale changes in herbivore-induced mRNAs. Plant Physiol. 2003, 131(4):1877-1893.
67. Afzal A.J., Wood A.J., Lightfoot D.A. Plant receptor-like serine threonine kinases: roles in signaling and plant defence. Mol. Plant Microbe Interact. 2008, 21(5):507-517.
68. Wang X., Zafian P., Choudhary M., Lawton M. The PR5K receptor protein kinase from Arabidopsis thaliana is structurally related to a family of plant defence proteins. Proc. Natl. Acad. Sci. U.S.A. 1996, 93(6):2598-2602.
69. Di Gaspero G., Cipriani G. Nucleotide binding site/leucine-rich repeats, Pto-like and receptor-like kinases related to disease resistance in grapevine. Mol. Genet. Genomics 2003, 269(5):612-623.
70. Schäfer S., Schmülling T. The CRK1 receptor-like kinase gene of tobacco is negatively regulated by cytokinin. Plant Mol. Biol. 2002, 50(2):155-166.
71. Dangl J.L., Jones J.D. Plant pathogens and integrated defence responses to infection. Nature 2001, 411:826-833.
72. Thomma B.P., Penninckx I.A., Broekaert W.F., Cammue B.P. The complexity of disease signaling in Arabidopsis. Curr. Opin. Immunol. 2001, 13(1):63-68.
73. Choi H.W., Kim Y.J., Lee S.C., Hong J.K., Hwang B.K. Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defence response to bacterial pathogens. Plant Physiol. 2007, 145(3):890-904.
74. Ashtamker C., Kiss V., Sagi M., Davydov O., Fluhr R. Diverse subcellular locations of cryptogein-induced reactive oxygen species production in tobacco Bright Yellow-2 cells. Plant Physiol. 2007, 143(4):1817-1826.
75. Durrant W.E., Rowland O., Piedras P., Hammond-Kosack K.E., Jones J.D. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 2000, 12(6):963-977.
76. Hückelhoven R. Cell wall-associated mechanisms of disease resistance and susceptibility. Annu. Rev. Phytopathol. 2007, 45:101-127.
77. Kieffer F., Lherminier J., Simon-Plas F., Nicole M., Paynot M., Elmayan T., Blein J.P. The fungal elicitor cryptogein induces cell wall modifications on tobacco cell suspension. J. Exp. Bot. 2000, 51(352):1799-1811.
78. Lherminier J., Benhamou N., Larrue J., Milat M.L., Boudon-Padieu E., Nicole M., Blein J.P. Cytological characterization of elicitin-induced protection in tobacco plants infected by Phytophthora parasitica or Phytoplasma. Phytopathology 2003, 93(10):1308-1319.
79. Vogel J.P., Raab T.K., Schiff C., Somerville S.C. PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell 2002, 14(9):2095-2106.
80. Lionetti V., Raiola A., Camardella L., Giovane A., Obel N., Pauly M., Favaron F., Cervone F., Bellincampi D. Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by Botrytis cinerea. Plant Physiol. 2007, 143(4):1871-1880.
81. An S.H., Choi H.W., Hong J.K., Hwang B.K. Regulation and function of the pepper pectin methylesterase inhibitor (CaPMEI1) gene promoter in defence and ethylene and methyl jasmonate signaling in plants. Planta 2009, 230(6):1223-1237.
82. Rose J.K., Braam J., Fry S.C., Nishitani K. The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol. 2002, 43(12):1421-1435.
83. Cosgrove D.J. Growth of the plant cell wall. Nat. Rev. Mol. Cell Biol. 2005, 6:850-861.
84. Li Y., Jones L., McQueen-Mason S. Expansins and cell growth. Curr. Opin. Plant Biol. 2003, 6(6):603-610.
85. Kawalleck P., Schmelzer E., Hahlbrock K., Somssich I.E. Two pathogen-responsive genes in parsley encode a tyrosine-rich hydroxyproline-rich glycoprotein (hrgp) and an anionic peroxidase. Mol. Gen. Genet. 1995, 247(4):444-452.
86. García-Muniz N., Martínez-Izquierdo J.A., Puigdomènech P. Induction of mRNA accumulation corresponding to a gene encoding a cell wall hydroxyproline-rich glycoprotein by fungal elicitors. Plant Mol. Biol. 1998, 38(4):623-632.
87. Lawton M.A., Lamb C.J. Transcriptional activation of plant defence genes by fungal elicitor, wounding, and infection. Mol. Cell. Biol. 1987, 7(1):335-341.
88. Schmelzer E., Kruger-Lebus S., Hahlbrock K. Temporal and spatial patterns of gene expression around sites of attempted fungal infection in parsley leaves. Plant Cell 1989, 1(10):993-1001.
89. Tronchet M., Balagué C., Kroj T., Jouanin L., Roby D. Cinnamyl alcohol dehydrogenases-C and D, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis. Mol. Plant Pathol. 2010, 11(1):83-92.
90. Tieman D., Taylor M., Schauer N., Fernie A.R., Hanson A.D., Klee H.J. Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde. Proc. Natl. Acad. Sci. U.S.A. 2006, 103(21):8287-8292.
91. Brock A., Brandt W., Dräger B. The functional divergence of short-chain dehydrogenases involved in tropinone reduction. Plant J. 2008, 54(3):388-401.
92. Nakajima K., Hashimoto T., Yamada Y. Two tropinone reductases with different stereospecificities are short-chain dehydrogenases evolved from a common ancestor. Proc. Natl. Acad. Sci. U.S.A. 1993, 90(20):9591-9595.
93. Dräger B. Tropinone reductases, enzymes at the branch point of tropane alkaloid metabolism. Phytochemistry 2006, 67(4):327-337.
94. Chaudhuri K., Das S., Bandyopadhyay M., Zalar A., Kollmann A., Jha S., Tepfer D. Transgenic mimicry of pathogen attack stimulates growth and secondary metabolite accumulation. Transgenic Res. 2009, 18(1):121-134.
95. Vögeli U., Chappell J. Induction of sesquiterpene cyclase and suppression of squalene synthetase activities in plant cell cultures treated with fungal elicitor. Plant Physiol. 1988, 88(4):1291-1296.
96. Rusterucci C., Stallaert V., Milat M.L., Pugin A., Ricci P., Blein J.P. Relationship between active oxygen species, lipid peroxidation, necrosis, and phytoalexin production induced by Elicitins in Nicotiana. Plant Physiol. 1996, 111(3):885-891.
97. Vögeli U., Vögeli-Lange R., Chappell J. Inhibition of phytoalexin biosynthesis in elicitor-treated tobacco cell-suspension cultures by calcium/calmodulin antagonists. Plant Physiol. 1992, 100(3):1369-1376.
98. Auldridge M.E., McCarty D.R., Klee H.J. Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr. Opin. Plant Biol. 2006, 9(3):315-321.
99. Ton J., Flors V., Mauch-Mani B. The multifaceted role of ABA in disease resistance. Trends Plant Sci. 2009, 14:310-317.
100. Braam J. Regulated expression of the calmodulin-related TCH genes in cultured Arabidopsis cells: induction by calcium and heat shock. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:3213-3216.
101. 2+-responsive cis elements in Arabidopsis. Plant Cell 2006, 18:2733-2748.
102. Choi H., Hong J., Ha J., Kang J., Kim S.Y. ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 2000, 275:1723-1730.
103. Choi M.S., Kim M.C., Yoo J.H., Moon B.C., Koo S.C., Park B.O., Lee J.H., Koo Y.D., Han H.J., Lee S.Y., Chung W.S., Lim C.O., Cho M.J. Isolation of a calmodulin-binding transcription factor from rice (Oryza sativa L.). J. Biol. Chem. 2005, 280:40820-40831.
104. Kim J., Kim H.Y. Functional analysis of a calcium-binding transcription factor involved in plant salt stress signaling. FEBS Lett. 2006, 580:5251-5256.