Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis

Plant Physiology

Volumn 140, Issue 4, 2006, Pages 1437-1450

  Wong, Chui E ^a   Li, Yong ^a   Labbe, Aurelie ^b   Guevara, David ^c   Nuin, Paulo ^c   Whitty, Brett ^c   Diaz, Claudia ^a   Golding, G Brian ^c   Gray, Gordon R ^d   Weretilnyk, Elizabeth A ^c   Griffith, Marilyn ^a   Moffatt, Barbara A ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

^d UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PHOTOSYNTHESIS; PLANTS (BOTANY); PROTEINS;

ARABIDOPSIS THALIANA; BIOTIC STRESS; PHOTOSYNTHETIC PROCESSES; THELLUNGIELLA SALSUGINEA;

BIODIVERSITY;

BIODIVERSITY; NUCLEIC ACIDS; PLANTS; PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; THELLUNGIELLA; THELLUNGIELLA SALSUGINEA;

EID: 33745454533     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.105.070508     Document Type: Article

References (71)

1. Al-Shehbaz IA, O'Kane SL Jr, Price RA (1999) Generic placement of species excluded from Arabidopsis (Brassicaceae). Novon 9: 296-307
2. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Olivia JD, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16: 3460-3479
3. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399
4. Audenaert K, De Meyer GB, Hofte MM (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol 128: 491-501
5. Baerr JN, Thomas JD, Taylor BG, Rodermel SR, Gray GR (2005) Differential photosynthetic compensatory mechanisms exist in the immutans mutant of Arabidopsis thaliana. Physiol Plant 124: 390-402
6. Balsamo RA, Willigen CV, Boyko W, Farrant J (2005) Retention of mobile water during dehydration in the desiccation-tolerant grass Eragrostis nindensis. Physiol Plant 124: 336-342
7. Bell E, Mullet JE (1993) Characterization of an Arabidopsis-lipoxygenase gene responsive to methyl jasmonate and wounding. Plant Physiol 103: 1133-1137
8. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate. A practical and powerful approach to multiple testing. J R Stat Soc Ser B 57: 289-300
9. Bray E (2002) Classification of genes differentially expressed during water-deficit stress in Arabidopsis thaliana: an analysis using microarray and differential expression data. Ann Bot (Lond) 89: 803-811
10. Bressan RA, Zhang C, Zhang H, Hasegawa P, Bohnert H, Zhu JK (2001) Learning from the Arabidopsis experience. The next gene search paradigm. Plant Physiol 127: 1354-1360
11. Bruxelles C, Peacock WJ, Dennis ES, Dolferus R (1996) Abscisic acid induces the alcohol dehydrogenase gene in Arabidopsis. Plant Physiol 111: 381-391
12. Cheong YH, Chang H, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129: 661-677
13. Cody WJ (2000) Flora of the Yukon Territory, Ed 2. NRC Research Press, Ottawa
14. Cosgrove DJ (2001) Wall structure and wall loosening. A look backwards and forwards. Plant Physiol 125: 131-134
15. Cui X, Kerr MK, Churchill GA (2003) Data transformation for cDNA microarray data. Stat Appl Genet Mol Biol 2: Article 4
16. Dudley RM, Haughton D (2002) Asymptotic normality with small relative errors of posterior probabilities of half-spaces. Ann Statist 30: 1311-1344
17. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14: 1675-1690
18. Gong Q, Li P, Ma S, Rupassara I, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison to its relative Arabidopsis thaliana. Plant J 44: 826-839
19. Gonzalez-Aguilar GA, Tiznado-Hernandez ME, Zavaleta-Gatica R, Martinez-Tellez MA (2004) Methyl jasmonate treatments reduce chilling injury and activate the defense response of guava fruits. Biochem Biophys Res Commun 313: 694-701
20. Gray GR, Heath D (2005) A global reorganization of the metabolome in Arabidopsis during cold acclimation is revealed by metabolic finger-printing. Physiol Plant 124: 236-248
21. Gray GR, Hope BJ, Qin X, Taylor BT, Whitehead CL (2003) The characterization of photoinhibition and recovery during cold acclimation in Arabidopsis thaliana using chlorophyll fluorescence imaging. Physiol Plant 119: 365-375
22. Gray GR, Savitch LV, Ivanov AG, Huner NPA (1996) Photosystem II excitation pressure and development of resistance to photoinhibition. II. Adjustment of photosynthetic capacity in winter wheat and winter rye. Plant Physiol 110: 61-71
23. Hong JK, Hwang BK (2002) Induction by pathogen, salt and drought of a basic class II chitinase mRNA and its in situ localization in pepper (Capsicum annuum). Physiol Plant 114: 549-558
24. Huner NPA, Öquist G, Hurry VM, Krol M, Falk S, Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37: 19-39
25. Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3: 224-230
26. Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K, Havaux M (2003) Early light-induced proteins protect Arabidopsis from photooxidative stress. Proc Natl Acad Sci USA 100: 4921-4926
27. Inan G, Zhang Q, Li PH, Wang ZL, Cao ZY, Zhang H, Zhang CQ, Quist TM, Goodwin SM, Zhu JH, et al (2004) Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135: 1718-1737
28. Jang JC, Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6: 1665-1679
29. Kendziorski CM, Newton MA, Lan H, Gould MN (2003) On parametric empirical Bayes methods for comparing multiple groups using replicated gene expression. Stat Med 22: 3899-3914
30. Krapp A, Hofmann B, Schafer C, Stitt M (1993) Regulation of the expression of rbcs and other photosynthetic genes by carbohydrates: a mechanism for the sink regulation of photosynthesis. Plant J 3: 817-828
31. Krapp A, Stitt M (1995) An evaluation of direct and indirect mechanisms for the sink-regulation of photosynthesis in spinach: changes in gas-exchange, carbohydrates, metabolites, enzyme-activities and steady-state transcript levels after cold-girdling source leaves. Planta 195: 313-323
32. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper J (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130: 2129-2141
33. Krol M, Ivanov AG, Jansson S, Kloppstech K, Huner NPA (1999) Greening under high light and cold temperature affects the level of xanthophyll-cycle pigments, early light-inducible proteins, and light-harvesting polypeptides in wild-type barley and the Chlorina f2 mutant. Plant Physiol 120: 193-203
34. Labbe A (2005) Multiple testing using the posterior probability of half-space: application to gene expression data. PhD thesis. University of Waterloo, Waterloo, ON, Canada
35. Labbe A, Thompson ME (2005) Hierarchical inverse Gaussian models and multiple testing: application to gene expression data. Stat Appl Genet Mol Biol 4: Article 23
36. Mantyla E, Lang V, Pavla ET (1995) Role of abscisic acid in drought-induced freezing tolerance, cold acclimation, and accumulation of LT178 and RAB18 proteins in Arabidopsis thaliana. Plant Physiol 107: 141-148
37. McDonald KL, Cahill DM (1999) Influence of abscisic acid and the abscisic acid biosynthesis inhibitor, norflurazon, on interactions between Phytophthora sojae and soybean (Glycine max). Eur J Plant Pathol 105: 651-658
38. Mohr PG, Cahill DM (2003) Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Funct Plant Biol 30: 461-469
39. Montané MH, Kloppstech K (2000) The family of light-harvesting- related proteins (LHCs, ELIPs, HLIPs): Was the harvesting of light their primary function? Gene 258: 1-8
40. Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125: 1558-1566
41. Nieuwland J, Feron R, Huisman BAH, Fasolino A, Hilbers CW, Derksen J, Mariani C (2005) Lipid transfer proteins enhance cell wall extension in tobacco. Plant Cell 17: 2009-2019
42. Nishitani K, Tominaga R (1992) Endo-xyloglucan transferase, a novel class of glycosyltransferase that catalyzes transfer of a segment of xyloglucan molecule to another xyloglucan molecule. J Biol Chem 267: 21058-21064
43. Orthen B, Popp M, Smirnoff N (1994) Hydroxyl radical scavenging properties of cyclitols. Proc R Soc Edinb Sect B (Biol) 102: 269-272
44. Penninckx IA, Thomma BP, Buchala A, Métraux J-P, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10: 2103-2113
45. Pharr DM, Stoop JMH, Williamson JD, Studer Feusi ME, Massel MO, Conkling MA (1995) The dual role of mannitol as osmoprotectant and photoassimilate in celery. Hortic Sci 30: 1182-1188
46. Potter E, Kloppstech K (1993) Effects of light stress on the expression of early light-inducible proteins in barley. Eur J Biochem 214: 779-786
47. Rathinasabapathi R (2000) Metabolic engineering for stress tolerance: installing osmoprotectant synthesis pathways. Ann Bot (Lond) 86: 709-716
48. Rezzonico E, Flury N, Meins F Jr, Beffa R (1998) Transcriptional down-regulation by abscisic acid of pathogenesis-related β-1,3-glucanase genes in tobacco cell cultures. Plant Physiol 117: 585-592
49. Richard S, Lapointe G, Rutledge RG, Seguin A (2000) Induction of chalcone synthase expression in white spruce by wounding and jasmonate. Plant Cell Physiol 41: 982-987
50. Seki M, Ishida J, Narusaka M, Fujita M, Nanjo T, Umezawa T, Kamiya A, Nakajima M, Enju A, Sakurai T, et al (2002a) Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct Integr Genomics 2: 282-329
51. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, et al (2002b) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high salinity stresses using a full length cDNA microarray. Plant J 31: 279-292
52. Sheen J (1994) Feedback-control of gene-expression. Photosynth Res 3: 427-438
53. Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6: 410-417
54. Steponkus PL (1984) Behavior of the plasma-membrane of isolated protoplasts during a freeze-thaw cycle. Cryobiology 21: 694-695
55. Stewart GR (1989) Desiccation injury, anhydrobiosis and survival. In HG Jones, TJ Flowers, MB Jones, eds, Plant under Stress. Cambridge University Press, Cambridge, UK, pp 115-130
56. Stitt M, Hurry V (2002) A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Curr Opin Plant Biol 5: 199-206
57. Strand A, Foyer CH, Gustafsson P, Gardeström P, Hurry V (2003) Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance. Plant Cell Environ 26: 523-535
58. Strand Å, Hurry V, Gustafsson P, Gardeström P (1997) Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant J 12: 605-614
59. Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu J-K, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135: 1697-1709
60. Tunnacliffe A, Lapinski J (2003) Resurrecting Van Leeuwenhoek's rotifers: a reappraisal of the role of disaccharides in anhydrobiosis. Philos Trans R Soc Lond B Biol Sci 358: 1755-1771
61. Volkov V, Wang B, Dominy PJ, Fricke W, Amtmann A (2004) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodium. Plant Cell Environ 27: 1-14
62. Wang ZI, Li PH, Fredricksen M, Gong ZH, Kim CS, Zhang CQ, Bohnert HJ, Zhu JK, Bressan RA, Hasegawa PM, et al (2004) Expressed sequence tags from Thellungiella halophila, a new model to study plant salt-tolerance. Plant Sci 166: 609-616
63. Ward EWB, Cahill DM, Bhattacharyya MK (1989) Abscisic acid suppression of phenylalanine ammonia-lyase activity and mRNA, and resistance of soybeans to Phytophthora megasperma f. sp. glycinea. Plant Physiol 91: 23-27
64. Warwick SI, Francis A, Mulligan GA (2004) Brassicaceae of Canada (contribution no. 981317.1225). Agriculture and Agri-Food Canada, Eastern Cereal and Oilseed Research Centre, Ottawa, ON, Canada
65. Wasternack C, Miersch O, Kramell R, Hause B, Ward J, Beale M, Boland W, Parthier B, Feussner I (1998) Jasmonic acid: biosynthesis, signal transduction, gene expression. Lipid-Fett 100: 139-146
66. Weretilnyk EA, Alexander KJ, Drebenstedt M, Snider JD, Summers PS, Moffatt BA (2001) Maintaining methylation activities during salt stress. The involvement of adenosine kinase. Plant Physiol 125: 856-865
67. Wong CE, Li Y, Whitty B, Akhter S, Diaz C, Brandle J, Golding B, Weretinylk E, Moffatt BA, Griffith M (2005) Expressed sequence tags from the Yukon ecotype of Thellungiella salsuginea reveal that gene expression in response to cold, drought and salinity shows little overlap. Plant Mol Biol 58: 561-574
68. Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25: 131-139
69. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53: 247-273
70. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621-2632
71. Zuther E, Buchel K, Hundertmark M, Stitt M, Hincha DK, Heyer AG (2004) The role of raffinose in the cold acclimation response of Arabidopsis thaliana. FEBS Lett 576: 169-173