Transcriptome analysis of Arabidopsis roots treated with signaling compounds: A focus on signal transduction, metabolic regulation and secretion

New Phytologist

Volumn 179, Issue 1, 2008, Pages 209-223

  Badri, Dayakar V ^a   Loyola Vargas, Victor M ^a,b   Du, Jiang ^a   Stermitz, Frank R ^a   Broeckling, Corey D ^a   Iglesias Andreu, Lourdes ^b,c   Vivanco, Jorge M ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b CENTRO DE INVESTIGACIÓN CIENTÍFICA DE YUCATÁN   (Mexico)

^c UNIVERSIDAD VERACRUZANA   (Mexico)

Author keywords

Arabidopsis; Defense response; Methyl jasmonate (MeJA); Nitric oxide (NO); Root secretion; Salicylic acid (SA); Signaling molecules; Transporters

Indexed keywords

ACETIC ACID DERIVATIVE; ARABIDOPSIS PROTEIN; CARRIER PROTEIN; CYCLOPENTANE DERIVATIVE; JASMONIC ACID METHYL ESTER; NITRIC OXIDE; OXYLIPIN; PHYTOHORMONE; SALICYLIC ACID;

GENE EXPRESSION; GENETIC ANALYSIS; HERB; LEAF; METABOLISM; MODELING; PLANT DEFENSE; SALICYLIC ACID; SECRETION; SIGNALING;

ARABIDOPSIS; ARTICLE; DNA MICROARRAY; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; MULTIGENE FAMILY; OXIDATION REDUCTION REACTION; PLANT EXUDATE; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECRETION; SIGNAL TRANSDUCTION;

ACETIC ACIDS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYCLOPENTANES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; MEMBRANE TRANSPORT PROTEINS; MULTIGENE FAMILY; NITRIC OXIDE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATION-REDUCTION; OXYLIPINS; PLANT EXUDATES; PLANT GROWTH REGULATORS; PLANT ROOTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALICYLIC ACID; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 44649154586     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2008.02458.x     Document Type: Article

References (80)

1. Badri DV, Loyola-Vargas VM, Broeckling CD, De la Peña C, Jasinski M, Santelia D, Martinoia E, Sumner LW, Banta LM, Stermitz FR et al. 2008. Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-binding cassette transporter mutants. Plant Physiology 146 : 762 771.
2. Bais HP, Park S-W, Weir T, Callaway RM, Vivanco JM. 2004. How plants communicate using the underground information superhighway. Trends in Plant Science 9 : 26 32.
3. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM. 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology 57 : 233 266.
4. Bednarek P, Schneider B, Svatos A, Oldham NJ, Hahlbrock K. 2005. Structural complexity, differential response to infection, and tissue specificity of indolic and phenylpropanoid secondary metabolism in Arabidopsis roots. Plant Physiology 138 : 1058 1070.
5. Beligni MV, Lamattina L. 1999. Nitric oxide protects against cellular damage produced by methylviologen herbicides in potato plants. Nitric Oxide 3 : 199 208.
6. Beligni MV, Lamattina L. 2000. Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210 : 215 221.
7. Bell E, Mullet JE. 1993. Characterization of an Arabidopsis lipoxygenase gene responsive to methyl jasmonate and wounding. Plant Physiology 103 : 1133 1137.
8. Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith DW, Benfey PN. 2003. A gene expression map of the Arabidopsis root. Science 302 : 1956 1960.
9. Brader G, Tas E, Palva ET. 2001. Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora. Plant Physiology 126 : 849 860.
10. van den Brûle S, Smart C. 2002. The plant PDR family of ABC transporters. Planta 216 : 95 106.
11. Campbell EJ, Schenk PM, Kazan K, Penninckx IAM, Anderson JP, Maclean DJ, Cammue BPA, Ebert PR, Manners JM. 2003. Pathogen-responsive expression of a putative ATP-binding cassette transporter gene conferring resistance to the diterpenoid sclareol is regulated by multiple defense signaling pathways in Arabidopsis. Plant Physiology 133 : 1272 1284.
12. Chen C, Chen Z. 2002. Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiology 129 : 706 716.
13. 2+-independent excretion modes of salicylic acid in tobacco cell suspension culture. Journal of Experimental Botany 52 : 1219 1226.
14. Cho K, Agrawal GK, Shibato J, Jung YH, Kim YK, Nahm BH, Jwa NS, Tamogami S, Han O, Kohda K et al. 2007. Survey of differentially expressed proteins and genes in jasmonic acid treated rice seedling shoot and root at the proteomics and transcriptomics levels. Journal of Proteome Research 6 : 3581 3603.
15. Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E et al. 1994. A central role of salicylic acid in plant disease resistance. Science 266 : 1247 1250.
16. Doughty KJ, Kiddle GA, Pye BJ, Wallsgrove RM, Pickett JA. 1995. Selective induction of glucosinolates in oilseed rape leaves by methyl jasmonate. Phytochemistry 38 : 347 350.
17. Farag MA, Huhman DV, Dixon RA, Sumner LW. 2008. Metabolomics reveals novel pathways, differential mechanistic and elicitor-specific responses in phenylpropanoid and isoflavonoid biosynthesis in Medicago truncatula cell cultures. Plant Physiology 146 : 387 402.
18. Farivar RS, Brecher P. 1996. Salicylate is a transcriptional inhibitor of the inducible nitric oxide synthase in cultured cardiac fibroblasts. Journal of Biological Chemistry 271 : 31585 31592.
19. Farmer EE, Almeras E, Krishnamurthy V. 2003. Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Current Opinion in Plant Biology 6 : 372 378.
20. Galis I, Simek P, Narisawa T, Sasaki M, Horiguchi T, Fukuda H, Matsuoka K. 2006. A novel R2R3 MYB transcription factor NtMYBJS1 is a methyl jasmonate-dependent regulator of phenylpropanoid-conjugate biosynthesis in tobacco. Plant Journal 46 : 573 592.
21. Gleba D, Borisjuk NV, Borisjuk LG, Kneer R, Poulev A, Sarzhinskaya M, Dushenkov S, Logendra S, Gleba YY, Raskin I. 1999. Use of plant roots for phytoremediation and molecular farming. Proceedings of the National Academy of Sciences, USA 96 : 5973 5977.
22. Grotewold E. 2005. Plant metabolic diversity: a regulatory perspective. Trends in Plant Science 10 : 57 62.
23. Grün S, Lindermayr C, Sell S, Durner J. 2006. Nitric oxide and gene regulation in plants. Journal of Experimental Botany 57 : 507 516.
24. Guo FQ, Okamoto M, Crawford NM. 2003. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302 : 100 103.
25. Halim VA, Vess A, Scheel D, Rosahl S. 2006. The role of salicylic acid and jasmonic acid in pathogen defense. Plant Biology 8 : 307 313.
26. He X-J, Mu R-L, Cao W-H, Zhang ZG, Zhang J-S, Chen S-Y. 2005. AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant Journal 44 : 903 916.
27. He ZH, Cheeseman I, He D, Kohorn B. 1999. A cluster of five cell wall-associated receptor kinase genes, Wak 1-5, are expressed in specific organs of Arabidopsis. Plant Molecular Biology 39 : 1189 1196.
28. Hendrawati O, Yao Q, Kim HK, Linthorst HJM, Erkelens C, Lefeber AWM, Choi YH, Verpoorte R. 2006. Metabolic differentiation of Arabidopsis treated with methyl jasmonate using nuclear magnetic resonance spectroscopy. Plant Science 170 : 1118 1124.
29. Hermann M, Kapiotis S, Hofbauer R, Exner M, Seelos C, Held I, Gmeiner B. 1999. Salicylate inhibits LDL oxidation initiated by superoxide/nitric oxide radicals. FEBS Letters 445 : 212 214.
30. Jung C, Lyou S, Yeu S, Kim M, Rhee S, Kim M, Lee J, Choi Y, Cheong JJ. 2007. Microarray-based screening of jasmonate-responsive genes in Arabidopsis thaliana. Plant Cell Reports 26 : 1053 1063.
31. Kaiser HF. 1960. The application of electronic computers to factor analysis. Educational and Psychological Measurement 20 : 141 151.
32. Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang SQ, Kachroo P et al. 2000. Nitric oxide and salicylic acid signaling in plant defense. Proceedings of the National Academy of Sciences, USA 97 : 8849 8855.
33. Kunkel BN, Brooks DM. 2002. Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology 5 : 325 331.
34. van Leeuwen H, Kliebenstein DJ, West MAL, Kim K, van Poecke R, Katagiri F, Michelmore RW, Doerge RW, Clair DA. 2007. Natural variation among Arabidopsis thaliana accessions for transcriptome response to exogenous salicylic acid. The Plant Cell 19 : 2099 2110.
35. Leshem YY, Pinchasov Y. 2000. Noninvasive photoacoustic spectroscopic determination of relative endogenous nitric oxide and ethylene content stoichiometry during the ripening of strawberries Fragaria anannasa (Duch.) and avocados Persea americana (Mill.). Journal of Experimental Botany 51 : 1471 1473.
36. Li L, Li C, Lee GI, Howe GA. 2002. Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proceedings of the National Academy of Sciences, USA 99 : 6416 6421.
37. Loyola-Vargas VM, Broeckling CD, Badri DV, Vivanco JM. 2007. Effect of transporters on the secretion of phytochemicals by the roots of Arabidopsis thaliana. Planta 225 : 301 310.
38. Mackerness SAH, John CF, Jordan B, Thomas B. 2001. Early signaling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Letters 489 : 237 242.
39. Melan MA, Dong X, Endara ME, Davis KR, Ausubel FM, Peterman TK. 1993. An Arabidopsis thaliana lipoxygenase gene can be induced by pathogens, abscisic acid, and methyl jasmonate. Plant Physiology 101 : 441 450.
40. Memelink J, Verpoorte R, Kijne JW. 2001. ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism. Trends in Plant Science 6 : 212 219.
41. Mikkelsen MD, Hansen CH, Wittstock U, Halkier BA. 2000. Cytochrome P450 CYP79B2 from Arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. Journal of Biological Chemistry 275 : 33712 33717.
42. Modolo LV, Cunha FQ, Braga MR, Salgado I. 2002. Nitric oxide synthase-mediated phytoalexin accumulation in soybean cotyledons in response to the Diaporthe phaseolorum f. sp. meridionalis elicitor. Plant Physiology 130 : 1288 1297.
43. Mueller LA, Zhang P, Rhee SY. 2003. AraCyc: a biochemical pathway database for Arabidopsis. Plant Physiology 132 : 453 460.
44. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15 : 473 497.
45. Murphy AM, Carr JP. 2002. Salicylic acid has cell-specific effects on tobacco mosaic virus replication and cell-to-cell movement. Plant Physiology 128 : 552 563.
46. Narasimhan K, Basheer C, Bajic VB, Swarup S. 2003. Enhancement of plant-microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiology 132 : 146 153.
47. Niki T, Mitsuhara I, Seo S, Ohtsubo N, Ohashi Y. 1998. Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant and Cell Physiology 39 : 500 507.
48. Parani M, Rudrabhatla S, Myers R, Weirich H, Smith B, Leaman DW, Goldman SL. 2004. Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotechnology Journal 2 : 359 366.
49. Parchmann S, Gundlach H, Mueller MJ. 1997. Induction of 12-oxo-phytodienoic acid in wounded plants and elicited plant cell cultures. Plant Physiology 115 : 1057 1064.
50. Park S-W, Kaimoyo E, Kumar D, Mosher S, Klessig DF. 2007. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318 : 113 116.
51. Peña-Cortés H, Albrecht T, Prat S, Weiler EW, Willmitzer L. 1993. Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191 : 123 128.
52. Penninckx IAM, Thomma BPHJ, Buchala A, Metraux JP, Broekaert WF. 1998. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. The Plant Cell 10 : 2103 2114.
53. Reymond P, Farmer EE. 1998. Jasmonate and salicylate as global signals for defense gene expression. Current Opinion in Plant Biology 1 : 404 441.
54. Rojo E, Titarenko E, León J, Berger S, Vancanneyt G, Sánchez-Serrano JJ. 1998. Reversible protein phosphorylation regulates jasmonic acid-dependent and -independent wound signal transduction pathways in Arabidopsis thaliana. Plant Journal 13 : 153 165.
55. Rouatt JW, Katznelson H. 1960. Influence of light on bacterial flora of roots. Nature 186 : 659 660.
56. Rouatt JW, Katznelson H, Payne TMB. 1960. Statistical evaluation of the rhizosphere effect. Soil Science Society of American Journal 24 : 271 273.
57. Routaboul JM, Kerhoas L, Debeaujon I, Pourcel L, Caboche M, Einhorn J, Lepiniec L. 2006. Flavonoid diversity and biosynthesis in seed of Arabidopsis thaliana. Planta 224 : 96 107.
58. Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K et al. 2005. Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant Journal 44 : 653 668.
59. Shah J. 2003. The salicylic acid loop in plant defense. Current Opinion in Plant Biology 6 : 365 371.
60. Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K et al. 2003. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. The Plant Cell 15 : 760 770.
61. Stohr C, Ullrich WR. 2002. Generation and possible roles of NO in plant roots and their apoplastic space. Journal of Experimental Botany 53 : 2293 2303.
62. Sugiyama A, Shitan N, Yazaki K. 2007. Involvement of a soybean ATP-binding cassette-type transporter in the secretion of genistein, a signal flavonoid in legume-rhizobium symbiosis. Plant Physiology 144 : 2000 2008.
63. Suzuki H, Srinivasa Reddy MS, Naoumkina M, Aziz N, May GD, Huhman DV, Sumner LW, Blount JW, Mendes P, Dixon RA. 2005. Methyl jasmonate and yeast elicitor induce differential transcriptional and metabolic re-programming in cell suspension cultures of the model legume Medicago truncatula. Planta 220 : 696 707.
64. Taguchi G, Yazawa T, Hayashida N, Okazaki M. 2001. Molecular cloning and heterologous expression of novel glucosyltransferases from tobacco cultured cells that have broad substrate specificity and are induced by salicylic acid and auxin. European Journal of Biochemistry 268 : 4086 4094.
65. Tamogami S, Rakwal R, Kodama O. 1997. Phytoalexin production elicited by exogenously applied jasmonic acid in rice leaves (Oryza sativa L.) is under the control of cytokinins and ascorbic acid. FEBS Letters 412 : 61 64.
66. Tan J, Bednarek P, Liu J, Schneider B, Svatos A, Hahlbrock K. 2004. Universally occurring phenylpropanoid and species-specific indolic metabolites in infected and uninfected Arabidopsis thaliana roots and leaves. Phytochemistry 65 : 691 699.
67. Thaler J, Karban R, Ullman D, Boege K, Bostock R. 2002. Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131 : 227 235.
68. Thomma BPHJ, Penninckx IAM, Cammue BPA, Broekaert WF. 2001. The complexity of disease signaling in Arabidopsis. Current Opinion in Immunology 13 : 63 68.
69. Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J. 1992. Acquired resistance in Arabidopsis. The Plant Cell 4 : 645 656.
70. Van der Fits L, Memelink J. 2000. ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289 : 295 257.
71. Vázquez-Flota F, Moreno-Valenzuela OA, Miranda-Ham ML, Coello-Coello J, Loyola-Vargas VM. 1994. Catharanthine and ajmalicine synthesis in Catharanthus roseus hairy root cultures. Medium optimization and elicitation. Plant Cell, Tissue and Organ Culture 38 : 273 279.
72. Veit M, Pauli GF. 1999. Major flavonoids from Arabidopsis thaliana leaves. Journal of Natural Products 62 : 1301 1303.
73. Wagner U, Edwards R, Dixon DP, Mauch F. 2002. Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Molecular Biology 49 : 515 532.
74. Walker TS, Bais HP, Grotewold E, Vivanco JM. 2003. Root exudation and rhizosphere biology. Plant Physiology 132 : 44 51.
75. Wendehenne D, Pugin A, Klessig DF, Durner J. 2001. Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends in Plant Science 6 : 177 183.
76. Wink DA, Mitchell JB. 1998. Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radical Biology and Medicine 25 : 434 456.
77. Xu MJ, Dong JF, Zhu MY. 2005. Nitric oxide mediates the fungal elicitor-induced hypericin production of Hypericum perforatum cell suspension cultures through a jasmonic-acid-dependent signal pathway. Plant Physiology 139 : 991 998.
78. 14C] jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris. Planta 203 : 436 441.
79. Zhao J, Davis LC, Verpoorte R. 2005. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances 23 : 283 333.
80. Zhao JA, Zhu WH, Hu Q. 2000. Enhanced ajmalicine production in Catharanthus roseus cell cultures by combined elicitor treatment: from shake-flask to 20-L airlift bioreactor. Biotechnology Letters 22 : 509 514.