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Gene expression profiles during heat acclimation in Arabidopsis thaliana suspension-culture cells

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Abstract

Thermotolerance is induced by moderated heat acclimation. Suspension cultures of heat-acclimated Arabidopsis thaliana L. (Heynh.), ecotype Columbia, show thermotolerance against lethal heat shock (9 min, 50°C), as evidenced by a chlorophyll assay and fluorescein diacetate staining. To monitor the genome-wide transcriptome changes induced by heat acclimation at 37°C, we constructed an A. thaliana cDNA microarray containing 7,989 unique genes, and applied it to A. thaliana suspension-culture cells harvested at various times (0.5, 1, 2.5, 6, and 16 h) during heat acclimation. Data analysis revealed 165 differentially expressed genes that were grouped into ten clusters. We compared these genes with published and publicly available microarray heat-stress-related data sets in AtGenExpress. Heat-shock proteins were strongly expressed, as previously reported, and we found several of the up-regulated genes encoded detoxification and regulatory proteins. Moreover, the transcriptional induction of DREB2 (dehydration responsive element-binding factor 2) subfamily genes and COR47/rd17 under heat stress suggested cross-talk between the signaling pathways for heat and dehydration responses.

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References

  • Adamska I, Kloppstech K (1991) Evidence for the localization of the nuclear-coded 22-kDa heat shock protein in a subfraction of thylakoid membranes. Eur J Biochem 198:375–381

    Article  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    PubMed  Google Scholar 

  • Asamizu E, Nakamura Y, Sato S, Tabata S (2000) A large scale analysis of cDNA in Arabidopsis thaliana: generation of 12,028 non-redundant expressed sequence tags from normalized and size-selected cDNA libraries. DNA Res 7:175–180

    Article  PubMed  Google Scholar 

  • Axelos M, Curie C, Mazzolini L, Bardet C, Lescure B (1992) A protocol for transient gene expression in Arabidopsis thaliana protoplasts isolated from cell suspension cultures. Plant Physiol Biochem 30:123–128

    Google Scholar 

  • Bailey TL, Elkan C (1995) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 3:21–29

    PubMed  Google Scholar 

  • Behl RK, Heise KP, Moawad AM (1996) High temperature tolerance in relation to changes in lipids in mutant wheat. Tropenlandwirt 97:131–135

    Google Scholar 

  • Burke JJ (2001) Identification of genetic diversity and mutations in higher plant acquired thermotolerance. Physiol Plant 112:167–170

    Article  Google Scholar 

  • Burke JJ, O’Mahony PJ, Oliver MJ (2000) Isolation of Arabidopsis thaliana mutants lacking components of acquired thermotolerance. Plant Physiol 123:575–588

    Article  PubMed  Google Scholar 

  • Busch W, Wunderlich M, Schoffl F (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J 41:1–14

    Article  PubMed  Google Scholar 

  • Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294–5299

    Article  PubMed  Google Scholar 

  • Clarke SM, Mur LA, Wood JE, Scott IM (2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J 38:432–447

    Article  PubMed  Google Scholar 

  • Criddle RS, Hopkin MS, McArthur ED, Hansen LD (1994) Plant distribution and the temperature-coefficient of metabolism. Plant Cell Environ 17:233–243

    Article  Google Scholar 

  • Dat JF, Foyer CH, Scott IM (1998) Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol 118:1455–1461

    Article  PubMed  Google Scholar 

  • Donaldson RP, Luster DG (1991) Multiple forms of plant cytochromes P450. Plant Physiol 96:669–674

    PubMed  Google Scholar 

  • Falcone DL, Ogas JP, Somerville CR (2004) Regulation of membrane fatty acid composition by temperature in mutants of Arabidopsis with alterations in membrane lipid composition. BMC Plant Biol 4:17

    Article  PubMed  Google Scholar 

  • Finkelstein D, Ewing R, Gollub J, Sterky F, Cherry JM, Somerville S (2002) Microarray data quality analysis: lessons from the AFGC project. Arabidopsis Functional Genomics Consortium. Plant Mol Biol 48:119–131

    Article  PubMed  Google Scholar 

  • Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54:767–781

    Article  PubMed  Google Scholar 

  • Goldsborough AP, Albrecht H, Stratford R (1993) Salicylic acid-inducible binding of a tobacco nuclear protein to a 10 bp sequence which is highly conserved amongst stress-inducible genes. Plant J 3:563–571

    Article  PubMed  Google Scholar 

  • Gong M, Li X-J, Dai X, Tian M, Li Z-G (1997) Involvement of calcium and calmodulin in the acquisition of HS induced thermotolerance in maize seedlings. J Plant Physiol 150:615–621

    Google Scholar 

  • Goyer A, Haslekas C, Miginiac-Maslow M, Klein U, Le Marechal P, Jacquot JP, Decottignies P (2002) Isolation and characterization of a thioredoxin-dependent peroxidase from Chlamydomonas reinhardtii. Eur J Biochem 269:272–282

    Article  PubMed  Google Scholar 

  • Hauser EJP, Morrison JH (1964) The cytochemical reduction of nitro blue tetrazolium as an index of pollen viability. Am J Bot 51:748–752

    Article  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300

    Article  PubMed  Google Scholar 

  • Hong SW, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci USA 97:4392–4397

    Article  PubMed  Google Scholar 

  • Howarth CJ (1991) Molecular responses of plants to an increased incidence of thermotolerance. Plant Cell Environ 14:831–841

    Article  Google Scholar 

  • Howarth CJ, Ougham HJ (1993) Gene expression under temperature stress. New Phytol 125:1–26

    Article  Google Scholar 

  • Huang B, Liu X, Fry JD (1998) Shoot physiological responses of two bentgrass cultivars to high temperature and poor soil aeration. Crop Sci 38:1219–1225

    Google Scholar 

  • Hugly S, Kunst L, Browse J, Somerville C (1989) Enhanced thermal tolerance of photosynthesis and altered chloroplast ultrastructure in a mutant of Arabidopsis deficient in lipid saturation. Plant Physiol 90:1134–1142

    PubMed  Google Scholar 

  • Jouanneau J-P, Péaud-Lenoёl C (1967) Croissance et synthèse des protéines de suspensions cellulaires de tabac sensibles á la kinétine. Physiol Plant 20:834–850

    Article  Google Scholar 

  • Kim SY, Hong CB, Lee I (2001) Heat shock stress causes stage-specific male sterility in Arabidopsis thaliana. J Plant Res 114:301–307

    Article  Google Scholar 

  • Kunst L, Browse J, Somerville C (1989) Enhanced thermal tolerance in a mutant of Arabidopsis deficient in palmitic acid unsaturation. Plant Physiol 91:401–408

    PubMed  Google Scholar 

  • Larkindale J, Huang B (2004) Changes of lipid composition and saturation level in leaves and roots for heat-stressed and heat-acclimated cree** bentgrass (Agrostis stolonifera). Environ Exp Bot 51:57–67

    Article  Google Scholar 

  • Lee JH, Hübel A, Schöffl F (1995) Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermotolerance in transgenic Arabidopsis. Plant J 8:603–612

    Article  PubMed  Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Article  PubMed  Google Scholar 

  • Lindquist S (1980) Varying patterns of protein synthesis in Drosophila during heat shock: implications for regulation. Dev Biol 77:463–479

    Article  PubMed  Google Scholar 

  • Liu X, Huang B (2000) Heat stress injury in relation to membrane lipid peroxidation in cree** bentgrass. Crop Sci 40:503–510

    Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    Article  PubMed  Google Scholar 

  • Maestri E, Klueva N, Perrotta C, Gulli M, Nguyen HT, Marmiroli N (2002) Molecular genetics of heat tolerance and heat shock proteins in cereals. Plant Mol Biol 48:667–681

    Article  PubMed  Google Scholar 

  • Malik MK, Slovin JP, Hwang CH, Zimmerman JL (1999) Modified expression of a carrot small heat shock protein gene, Hsp17.7, results in increased or decreased thermotolerance. Plant J 20:89–99

    Google Scholar 

  • Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38:982–993

    Article  PubMed  Google Scholar 

  • McCabe PF, Leaver CJ (2000) Programmed cell death in cell cultures. Plant Mol Biol 44:359–368

    Article  PubMed  Google Scholar 

  • McCabe PF, Levine A, Meijer PJ, Tapon NA, Pennell RI (1997) A programmed cell death pathway activated in carrot cells cultured at low cell density. Plant J 12:267–280

    Article  Google Scholar 

  • Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665

    Article  PubMed  Google Scholar 

  • Nover L, Scharf KD, Neumann D (1983) Formation of cytoplasmic heat shock granules in tomato cell cultures and leaves. Mol Cell Biol 3:1648–1655

    PubMed  Google Scholar 

  • Ong CK, Baker NR (1985) Temperature and leaf growth. In: Baker NR, Davies WJ, Ong CK (eds) Control of leaf growth. Seminar series, Society for Experimental Biology, No. 27. Cambridge University Press, Cambridge, pp 175–200

    Google Scholar 

  • Prestridge DS (1991) SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements. Comput Appl Biosci 7:203–206

    PubMed  Google Scholar 

  • Queitsch C, Hong SW, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12:479–492

    Article  PubMed  Google Scholar 

  • Restivo FM, Tassi F, Maestri E, Lorenzoni C, Puglisi PP, Marmiroli N (1986) Identification of chloroplast associated heat shock proteins in Nicotiana plumbaginifolia protoplasts. Curr Genet 11:145–149

    Article  Google Scholar 

  • Richmond T, Somerville S (2000) Chasing the dream: plant EST microarrays. Curr Opin Plant Biol 3:108–116

    Article  PubMed  Google Scholar 

  • Riviere JL, Cabbane F (1987) Animal and plant cytochrome P450 systems. Biochemie 69:743–752

    Article  Google Scholar 

  • Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathway collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696

    Article  PubMed  Google Scholar 

  • Robertson AJ, Ishikawa M, Gusta LV, MacKenzie SL (1994) Abscisic acid-induced heat tolerance in Bromus inermis Leyss cell-suspension cultures. Heat-stable, abscisic acid-responsive polypeptides in combination with sucrose confer enhanced thermostability. Plant Physiol 105:181–190

    Article  PubMed  Google Scholar 

  • Rombauts S, Florquin K, Lescot M, Marchal K, Rouze P, Van de Peer Y (2003) Computational approaches to identify promoters and cis-regulatory elements in plant genomes. Plant Physiol 132:1162–1176

    Article  PubMed  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009

    Article  PubMed  Google Scholar 

  • Schena M, Shalon D, Davis RW, Brown PO (1995) Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270:467–470

    PubMed  Google Scholar 

  • Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61–67

    Article  PubMed  Google Scholar 

  • Sharkey TD, Chen XY, Yeh S (2001) Isoprene increases thermotolerance of fosmidomycin-fed leaves. Plant Physiol 125:2001–2006

    Article  PubMed  Google Scholar 

  • Swidzinski JA, Sweetlove LJ, Leaver CJ (2002) A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J 30:431–446

    Article  PubMed  Google Scholar 

  • Takahashi T, Komeda Y (1989) Characterization of two genes encoding small heat-shock proteins in Arabidopsis thaliana. Mol Gen Genet 219:365–372

    Article  PubMed  Google Scholar 

  • Takahashi T, Naito S, Komeda Y (1992) Isolation and analysis of the expression of two genes for the 81-kilodalton heat shock proteins from Arabidopsis. Plant Physiol 99:383–397

    PubMed  Google Scholar 

  • Thomashow MF (2001) So what’s new in the field of plant cold acclimation? Lots! Plant Physiol 125:89–93

    Article  PubMed  Google Scholar 

  • Vallelian-Bindschedler L, Schweizer P, Mosinger E, Metraux J-P (1998) Heat induced resistance in barley to powdery mildew (Blumeria graminis f. sp. Hordei) is associated with a bust of AOS. Physiol Mol Plant Pathol 52:185–199

    Article  Google Scholar 

  • Vierling E (1991) The roles of heat shock protein in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620

    Article  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  PubMed  Google Scholar 

  • Yang KA, Lim CJ, Hong JK, ** ZL, Hong JC, Yun D-J, Chung WS, Lee SY, Cho MJ, Lim CO (2005) Identification of Chinese cabbage genes up-regulated by prolonged cold by using microarray analysis. Plant Sci 168:959–966

    Article  Google Scholar 

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Acknowledgements

This research was supported by grants from the Environmental Biotechnology National Core Research Center Program (R15-2003-012-01001-0), KOSEF/MOST, and the Biogreen 21 Program, RDA, Republic of Korea. C.J. Lim is a recipient of a scholarship from the BK 21 Program granted by ME & HRD, Republic of Korea.

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  1. Division of Applied Life Science (BK21), Environmental Biotechnology National Core Research Center and PMBBRC, Gyeongsang National University, **ju, 660-701, Korea

    Chan Ju Lim, Kyung Ae Yang, Joon Ki Hong, ** Soo Choi, Dea-** Yun, Jong Chan Hong, Woo Sik Chung, Sang Yeol Lee, Moo Je Cho & Chae Oh Lim

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  1. Chan Ju Lim
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Lim, C.J., Yang, K.A., Hong, J.K. et al. Gene expression profiles during heat acclimation in Arabidopsis thaliana suspension-culture cells. J Plant Res 119, 373–383 (2006). https://doi.org/10.1007/s10265-006-0285-z

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