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Gene-expression profiling of grape bud response to two alternative dormancy-release stimuli expose possible links between impaired mitochondrial activity, hypoxia, ethylene-ABA interplay and cell enlargement

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Abstract

A grape-bud-oriented genomic platform was produced for a large-scale comparative analysis of bud responses to two stimuli of grape-bud dormancy release, hydrogen cyanamide (HC) and heat shock (HS). The results suggested considerable similarity in bud response to the stimuli, both in the repertoire of responding genes and in the temporary nature of the transcriptome reprogramming. Nevertheless, the bud response to HC was delayed, more condensed and stronger, as reflected by a higher number of regulated genes and a higher intensity of regulation compared to the response to HS. Integrating the changes occurring in response to both stimuli suggested perturbation of mitochondrial activity, development of oxidative stress and establishment of a situation that resembles hypoxia, which coincides with induction of glycolysis and fermentation, as well as changes in the interplay between ABA and ethylene metabolism. The latter is known to induce various growth responses in submerged plants and the possibility of a similar mechanism operating in the bud meristem during dormancy release is raised. The new link suggested between sub lethal stress, mitochondrial activity, hypoxic conditions, ethylene metabolism and cell enlargement during bud dormancy release may be instrumental in understanding the dormancy-release mechanism. Temporary increase of acetaldehyde, ethanol and ethylene in response to dormancy release stimuli demonstrated the predictive power of the working model, and its relevance to dormancy release was demonstrated by enhancement of bud break by exogenous ethylene and its inhibition by an ethylene signal inhibitor.

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References

  • Baud S, Vaultier MN, Rochat C (2004) Structure and expression of the sucrose synthase multigene family in Arabidopsis. J Exp Bot 396:397–409

    Article  Google Scholar 

  • Baxter CJ, Redestig H, Schauer N, Repsilber D, Patil KR, Nielsen J, Selbig J, Liu J, Fernie AR, Sweetlove LJ (2007) The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol 143:312–325

    Article  PubMed  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B Met 57:289–300

    Google Scholar 

  • Benschop JJ, Jackson MB, Gühl K, Vreeburg RA, Croker SJ, Peeters AJ, Voesenek LA (2005) Contrasting interactions between ethylene and abscisic acid in Rumex species differing in submergence tolerance. Plant J 44:756–768

    Article  PubMed  CAS  Google Scholar 

  • Benschop JJ, Bou J, Peeters AJ, Wagemaker N, Gühl K, Ward D, Hedden P, Moritz T, Voesenek LA (2006) Long-term submergence-induced elongation in Rumex palustris requires abscisic acid-dependent biosynthesis of gibberellin. Plant Physiol 141:1644–1652

    Article  PubMed  CAS  Google Scholar 

  • Beveridge CA, Mathesius U, Rose RJ, Gresshoff PM (2007) Common regulatory themes in meristem development and whole-plant homeostasis. Curr Opin Plant Biol 10:44–51

    Article  PubMed  CAS  Google Scholar 

  • Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville

    Google Scholar 

  • Chen G, Hu Z, Grierson D (2008) Differential regulation of tomato ethylene responsive factor LeERF3b, a putative repressor, and the activator Pti4 in ripening mutants and in response to environmental stresses. J Plant Physiol 165:662–670

    Article  PubMed  CAS  Google Scholar 

  • Clifton R, Millar AH, Whelan J (2006) Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. Biochim Biophys Acta 1757:730–741

    Article  PubMed  CAS  Google Scholar 

  • Cox MC, Benschop JJ, Vreeburg RA, Wagemaker CA, Moritz T, Peeters AJ, Voesenek LA (2004) The role of ethylene, auxin, abscisic acid, and gibberellin in the hyponastic growth of submerged Rumex palustris petioles. Plant Physiol 136:2948–2960

    Article  PubMed  CAS  Google Scholar 

  • Crawford RMM (1977) Tolerance of anoxia and ethanol metabolism in germinating seeds. New Phytol 79:511–517

    Article  CAS  Google Scholar 

  • Dokoozlian NK (1999) Chilling temperature and duration interact on the bud break of ‘perlette’ grapevine cuttings. HortScience 34:1054–1056

    Google Scholar 

  • Dokoozlian NZ, Williams Wang LE, Neja RA (1995) Chilling exposure and hydrogen cyanamide interact in breaking dormancy of grape buds. HortScience 30:1244–1247

    CAS  Google Scholar 

  • El-Shereif AR, Mizutani F, Onguso JM, Sharif Hossain ABM (2005) Effect of different temperatures and sampling dates on bud break and ACC content of ‘Muscate Baily A’ grapevine buds. Int J Bot 1:34–37

    Article  Google Scholar 

  • Erez A (1987) Chemical control of bud break. HortScience 22:1240–1243

    CAS  Google Scholar 

  • Erez A (1995) Means to compensate for insufficient chilling to improve bloom and leafing. Acta Hort 395:81–95

    Google Scholar 

  • Erez A, Lavee S (1974) Recent advances in breaking the dormancy of deciduous fruit trees. Proceedings of the 19th international horticulture congress, Warszaw, Poland, vol 3, pp 69–78

  • Faust M, Erez A, Rowland IJ, Wang SY, Norman HA (1997) Bud dormancy in perennial fruit trees: physiological basis for dormancy induction, maintenance, and release. HortScience 32:623–628

    Google Scholar 

  • Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80

    Article  PubMed  Google Scholar 

  • George AP, Nissen RJ, Baker JA (1986) Low chill peach and nectarine cultivars. Qld Agric J 112:27–33

    Google Scholar 

  • Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P (2000) Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 12:1117–1126

    Article  PubMed  CAS  Google Scholar 

  • Gu R, Fonseca S, Puskas LG, Hackler L Jr, Zvara A, Dudits D, Pais MS (2004) Transcript identification and profiling during salt stress and recovery of Populus euphratica. Tree Physiol 24:265–276

    PubMed  CAS  Google Scholar 

  • Hacham Y, Schuster G, Amir R (2006) An in vivo internal deletion in the N-terminus region of Arabidopsis cystathionine gamma-synthase results in CGS expression that is insensitive to methionine. Plant J 45:955–967

    Article  PubMed  CAS  Google Scholar 

  • Halaly T, Pang X, Batikoff T, Keilin T, Crane O, Keren A, Venkateswari J, Ogrodovitch A, Or E (2008) Similar mechanisms are triggered by alternative external stimuli that induce dormancy release: comparative study of the effects of hydrogen cyanamide and heat shock on dormancy release in grape buds. Planta 228:79–88

    Article  PubMed  CAS  Google Scholar 

  • Hao D, Ohme-Takagi M, Sarai A (1998) Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element-binding factor (ERF domain) in plants. J Biol Chem 273:26857–26861

    Article  PubMed  CAS  Google Scholar 

  • Hatzivassiliou G, Zhao F, Bauer DE, Andreadis C, Shaw AN, Dhanak D, Hingorani SR, Tuveson DA, Thompson CB (2005) ATP citrate lyase inhibition can suppress tumor cell growth. Cancer Cell 8:311–321

    Article  PubMed  CAS  Google Scholar 

  • Horvath DP, Chao WS, Anderson JV (2002) Molecular analysis of signals controlling dormancy and growth in underground adventitious buds of leafy spurge. Plant Physiol 128:1439–1446

    Article  PubMed  CAS  Google Scholar 

  • Huber W, von Heydebreck A, Sueltmann H, Poustka A, Vingron M (2002) Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18:S96–S104

    PubMed  Google Scholar 

  • Igamberdiev AU, Seregelyes C, Manach N, Hill RD (2004) NADH-dependent metabolism of nitric oxide in alfalfa root cultures expressing barley hemoglobin. Planta 219:95–102

    Article  PubMed  CAS  Google Scholar 

  • Iwasaki K (1980) Effects of bud scale removal, calcium cyanamide, GA3, and ethephon on bud break of ‘Muscat of Alexandria’ grape (Vitis vinifera L.). J Jpn Soc Hort Sci 48:395–398

    Article  CAS  Google Scholar 

  • Iwasaki K (1981) Effects of bud scale removal, calcium cyanamide, GA3, and ethaphon on bud break of ‘Musxat of Alexandria’ grape (Vitis vinifera L.). Japan Soc Hort Sci 48:395–398

    Article  Google Scholar 

  • Katz YS, Galili G, Amir R (2006) Regulatory role of cystathionine-gamma-synthase and de novo synthesis of methionine in ethylene production during tomato fruit ripening. Plant Mol Biol 61:255–268

    Article  PubMed  CAS  Google Scholar 

  • Keilin T, Pang X, Venkateswari J, Halaly T, Crane O, Keren A, Ogrodovitch A, Ophir R, Volpin H, Galbraith D, Or E (2007) Digital expression profiling of a grape-bud EST collection leads to new insight into molecular events during grape-bud dormancy release. Plant Sci 173:446–457

    Article  CAS  Google Scholar 

  • Kende H, van der Knaap E, Cho HT (1998) Deepwater rice: a model plant to study stem elongation. Plant Physiol 118:1105–1110

    Article  PubMed  CAS  Google Scholar 

  • Klingenberg M (1989) Molecular aspects of adenine nucleotide carrier from mitochondria. Arch Biochem Biophys 270:1–14

    Article  PubMed  CAS  Google Scholar 

  • Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246

    Article  PubMed  CAS  Google Scholar 

  • Koussa T, Broquedis M, Bouard J (1994) Changes of abscisic acid level during the development of grapevine latent buds, particularly in the phase of dormancy break. Vitis 33:63–67

    CAS  Google Scholar 

  • Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473

    Article  PubMed  CAS  Google Scholar 

  • Lang GA (1987) Dormancy: a new universal terminology. HortScience 22:817–820

    Google Scholar 

  • Lasanthi-Kudahettige R, Magneschi L, Loreti E, Gonzali S, Licausi F, Novi G, Beretta O, Vitulli F, Alpi A, Perata P (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiol 144:218–231

    Article  PubMed  CAS  Google Scholar 

  • Lavee S, May P (1997) Dormancy of grapevine buds. Aust J Grape Wine Res 3:31–46

    Article  CAS  Google Scholar 

  • Liotenberg S, North H, Marion-Poll A (1999) Molecular biology and regulation of abscisic acid biosynthesis in plants. Plant Physiol Biochem 37:341–350

    Article  CAS  Google Scholar 

  • Liu F, Vantoai T, Moy LP, Bock G, Linford LD, Quackenbush J (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol 137:1115–1129

    Article  PubMed  CAS  Google Scholar 

  • Marana C, Garcia-Olmedo F, Carbonero P (1990) Differential expression of two types of sucrose synthase-encoding genes in wheat in response to anaerobiosis, cold shock and light. Gene 88:167–172

    Article  PubMed  CAS  Google Scholar 

  • Mathiason K, He D, Grimplet J, Venkateswari J, Galbraith DW, Or E, Fennell A (2008) Transcript profiling in Vitis riparia during chilling requirement fulfillment reveals coordination of gene expression patterns with optimized bud break. Funct Integr Genomics PMID: 18633655

  • Mazzitelli L, Hancock RD, Haupt S, Walker PG, Pont SDA, McNicol J, Cardle L, Morris J, Viola R, Brennan R, Hedley PE, Taylor MA (2007) Co-ordinated gene expression during phases of dormancy release in raspberry (Rubus idaeus L.) buds. J Exp Bot 58:1035–1045

    Article  PubMed  CAS  Google Scholar 

  • Métraux JP, Kende H (1983) The role of ethylene in the growth response of submerged deepwater rice. Plant Physiol 72:441–446

    Article  PubMed  Google Scholar 

  • Mizutani F, Hino A, Amano S, Kadoya K, Watanabe J, Akiyoshi H (1995) Effect of calcium cyanamide, GA3 and scale removal on bud break, ethylene production and ACC content in grapevine buds. Memoirs of the College of Agriculture, Ehime University, vol 40, pp 91–97

  • Moller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591

    Article  PubMed  CAS  Google Scholar 

  • Nie X, Hill RD (1997) Mitochondrial respiration and hemoglobin gene expression in barley aleurone tissue. Plant Physiol 114:835–840

    PubMed  CAS  Google Scholar 

  • Nir G, Lavee S (1993) Metabolic changes during cyanimide induced dormancy release in grapevines. Acta Hort 329:271–274

    Google Scholar 

  • Nir G, Shulman Y, Fanberstein L, Lavee S (1986) Changes in the activity of catalase (EC 1.11.1.6) in relation to the dormancy of grapevine (Vitis vinifera L.) buds. Plant Physiol 81:1140–1142

    Article  PubMed  CAS  Google Scholar 

  • Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182

    Article  PubMed  CAS  Google Scholar 

  • Olsen JE (2003) Molecular and physiological mechanisms of bud dormancy regulation. Acta Hort 618:437–453

    CAS  Google Scholar 

  • Or E, Nir G, Vilozny I (1999) Timing of hydrogen cyanamide application to grapevine buds. Vitis 38:1–6

    CAS  Google Scholar 

  • Or E, Belausov E, Popilevsky I, Ben Tal Y (2000a) Changes in endogenous ABA level in relation to the dormancy cycle in grapevine grown in hot climate. J Horti Sci Biotechnol 75:190–194

    CAS  Google Scholar 

  • Or E, Vilozny I, Eyal Y, Ogrodovitch A (2000b) The transduction of the signal for grape bud dormancy breaking, induced by hydrogen cyanamide, may involve the SNF-like protein kinase GDBrPK. Plant Mol Biol 43:483–489

    Article  PubMed  CAS  Google Scholar 

  • Or E, Vilozny I, Fennell A, Eyal Y, Ogrodovitch A (2002) Dormancy in grape buds: isolation and characterization of catalase cDNA and analysis of its expression following chemical induction of bud dormancy release. Plant Sci 162:121–130

    Article  CAS  Google Scholar 

  • Oracz K, El-Maarouf-Bouteau H, Bogatek R, Corbineau F, Bailly C (2008) Release of sunflower seed dormancy by cyanide: cross-talk with ethylene signalling pathway. J Exp Bot 59:2241–2251

    Article  PubMed  CAS  Google Scholar 

  • Oracz K, El-Maarouf-Bouteau H, Kranner I, Bogatek R, Corbineau F, Bailly C (2009) The mechanisms involved in seed dormancy alleviation by hydrogen cyanide unravel the role of reactive oxygen species as key factors of cellular signalling during germination. Plant Physiol (Epub ahead of print)

  • Pacey-Miller T, Scott K, Ablett E, Tingey S, Ching A, Henry R (2003) Genes associated with the end of dormancy in grapes. Funct Integr Genomics 3:144–152

    Article  PubMed  CAS  Google Scholar 

  • Pang X, Halaly T, Crane O, Keilin T, Keren A, Ogrodovitch A, Galbraith D, Or E (2007) Involvement of calcium signaling in dormancy release of grape buds. J Exp Bot 58:3249–3262

    Article  PubMed  CAS  Google Scholar 

  • Patel M, Day BJ, Crapo JD, Fridovich I, McNamara JO (1996) Requirement for superoxide in excitotoxic cell death. Neuron 16:345–355

    Article  PubMed  CAS  Google Scholar 

  • Peeters AJ, Cox MC, Benschop JJ, Vreeburg RA, Bou J, Voesenek LA (2002) Submergence research using Rumex palustris as a model: looking back and going forward. J Exp Bot 53:391–398

    Article  PubMed  CAS  Google Scholar 

  • Perez FJ, Lira W (2005) Possible role of catalase in post-dormancy bud break in grapevines. J Plant Physiol 162:301–308

    Article  PubMed  CAS  Google Scholar 

  • Perez FJ, Rubio S, Ormeno-Nunez J (2007) Is erratic bud-break in grapevines grown in warm winter areas related to disturbances in mitochondrial respiratory capacity and oxidative metabolism? Funct Plant Biol 34:624–632

    Article  CAS  Google Scholar 

  • Perez FJ, Vergara S, Rubio S (2008) H2O2 is involved in the dormancy-breaking effect of hydrogen cyanamide in grapevine buds. Plant Growth Regul 55:149–155

    Article  CAS  Google Scholar 

  • Pesis E, Marinansky R, Zauberman G, Fuchs Y (1994) Prestorage low-oxygen atmosphere treatment reduces chilling injury symptoms in Fuerte avocado fruit. HortScience 29:1042–1046

    Google Scholar 

  • Pirrello J, Jaimes-Miranda F, Sanchez-Ballesta MT, Tournier B, Khalil-Ahmad Q, Regad F, Latché A, Pech JC, Bouzayen M (2006) Sl-ERF2, a tomato ethylene response factor involved in ethylene response and seed germination. Plant Cell Physiol 47:1195–1205

    Article  PubMed  CAS  Google Scholar 

  • Rehling P, Pfanner N, Meisinger C (2003) Insertion of hydrophobic membrane proteins into the inner mitochondrial membrane—a guided tour. J Mol Biol 326:639–657

    Article  PubMed  CAS  Google Scholar 

  • Ricoult C, Echeverria LO, Cliquet JB, Limami AM (2006) Characterization of alanine aminotransferase (AlaAT) multigene family and hypoxic response in young seedlings of the model legume Medicago truncatula. J Exp Bot 57:3079–3089

    Article  PubMed  CAS  Google Scholar 

  • Ruonala R, Rinne PLH, Baghour M, Moritz T, Tuominen H, Kangasjärvi J (2006) Transitions in the functioning of the shoot apical meristem in birch (Betula pendula) involve ethylene. Plant J 46:628–640

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Saure M (1985) Dormancy release in deciduous fruit trees. Hort Rev 7:239–300

    Google Scholar 

  • Schrader J, Moyle R, Bhalerao R, Hertzberg M, Lundeberg J, Nilsson P, Bhalerao RP (2004) Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J 40:173–187

    Article  PubMed  CAS  Google Scholar 

  • Sharma V, Suvarna R, Meganathan R, Hudspeth MES (1992) Menaquinone (Vitamin K2) biosynthesis: nucleotide sequence and expression of the memB gene from Escherichia coli. J Bacteriol 174:5057–5062

    PubMed  CAS  Google Scholar 

  • Shulman Y, Nir G, Fanberstein L, Lavee S (1983) The effect of cyanamide on the release from dormancy of grapevine buds. Sci Hort 19:97–104

    Article  CAS  Google Scholar 

  • Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Gen Mol Biol 3: article 3

  • Smyth GK (2005) Paper 116: Individual channel analysis of two-colour microarrays. In 55th Session of the International Statistics Institute, 5–12 April 2005, Sydney Convention & Exhibition Centre, Sydney, Australia (CD). International Statistical Institute, Bruxelles

  • Smyth GK, Michaud J, Scott HS (2005) Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21:2067–2075

    Article  PubMed  CAS  Google Scholar 

  • Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12:3703–3714

    Article  PubMed  CAS  Google Scholar 

  • Song CP, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu JK (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17:2384–2396

    Article  PubMed  CAS  Google Scholar 

  • Steffens B, Wang J, Sauter M (2006) Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 223:604–612

    Article  PubMed  CAS  Google Scholar 

  • Subbaiah CC, Sachs MM (2003) Molecular and cellular adaptations of maize to flooding stress. Ann Bot 91:119–127

    Article  PubMed  CAS  Google Scholar 

  • Sun T, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55:197–223

    Article  PubMed  CAS  Google Scholar 

  • Suttle JC (1998) Postharvest changes in endogenous cytokinins and cytokinin efficacy in potato tubers in relation to bud endodormancy. Physiol Plant 103:59–69

    Article  CAS  Google Scholar 

  • Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant J 32:891–904

    Article  PubMed  CAS  Google Scholar 

  • Tabuchi A, Funaji K, Nakatsubo J, Fukuchi M, Tsuchiya T, Tsuda M (2003) Inactivation of aconitase during the apoptosis of mouse cerebellar granule neurons induced by a deprivation of membrane depolarization. J Neurosci Res 71:504–515

    Article  PubMed  CAS  Google Scholar 

  • Taylor ER, Nie XZ, MacGregor AW, Hill RD (1994) A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions. Plant Mol Biol 24:853–862

    Article  PubMed  CAS  Google Scholar 

  • Tohbe M, Mochioka R, Horiuchi S, Ogata T, Shiozaki S, Kurooka H (1998) Role of ACC and glutathione during breaking of dormancy in grapevine buds by high temperature treatment. J Japan Soc Hort Sci 67:897–901

    Article  CAS  Google Scholar 

  • Tournier B, Sanchez-Ballesta MT, Jones B, Pesquet E, Regad F, Latché A, Pech JC, Bouzayen M (2003) New members of the tomato ERF family show specific expression pattern and diverse DNA-binding capacity to the GCC box element. FEBS Lett 550:149–154

    Article  PubMed  CAS  Google Scholar 

  • Voesenek LA, Banga M, Their RH, Mudde CM, Harren FJ, Barendse GW, Blom CW (1993) Submergence-induced ethylene synthesis, entrapment, and growth in two plant species with contrasting flooding resistances. Plant Physiol 103:783–791

    PubMed  CAS  Google Scholar 

  • Wang SY, Jiao HJ, Faust M (1991a) Changes in ascorbate, glutathione, and related enzyme activities during thidiazuron-induced bud break of apple. Physiol Plant 82:231–236

    Article  CAS  Google Scholar 

  • Wang SY, Jiao HJ, Faust M (1991b) Changes in metabolic enzyme activities during thidiazuron-induced lateral budbreak of apple. HortScience 82:231–236

    CAS  Google Scholar 

  • Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30:e15

    Article  PubMed  Google Scholar 

  • Zegzouti H, Jones B, Frasse P, Marty C, Maitre B, Latch A, Pech JC, Bouzayen M (1999) Ethylene-regulated gene expression in tomato fruit: characterization of novel ethylene-responsive and ripening-related genes isolated by differential display. Plant J 18:589–600

    Article  PubMed  CAS  Google Scholar 

  • Zentella R, Zhang ZL, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, Sun TP (2007) Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19:3037–3057

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Huang Z, Xie B, Chen Q, Tian X, Zhang X, Zhang H, Lu X, Huang D, Huang R (2004) The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco. Planta 220:262–270

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Fruit Tree Sciences, Institute of Horticulture, Agricultural Research Organization, The Volcani Center, Bet Dagan, 50250, Israel

    Ron Ophir, Xuequn Pang, Tamar Halaly, Shimon Lavee & Etti Or

  2. College of Life Science, South China Agricultural University, Guangzhou, 510642, China

    Xuequn Pang

  3. Department of Plant Sciences and Bios Institute, University of Arizona, Tucson, AZ, 85721, USA

    Jaganatha Venkateswari & David Galbraith

  4. Department of Botany and Plant Sciences, 2150 Batchelor Hall, University of California, Riverside, CA, 92521, USA

    Jaganatha Venkateswari

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  1. Ron Ophir
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Correspondence to Etti Or.

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This research was supported by Research Grant Award No. IS-3340-02 from BARD, The United States-Israel Binational Agricultural Research and Development Fund.

Ron Ophir, Xuequn Pang, Tamar Halaly, and Jaganatha Venkateswari contributed equally to the paper.

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Description of clone-to-gene analysis and content of file S2 and S3. (XLS 6436 kb)

Clones differential expression analysis results. (DOC 69 kb)

11103_2009_9531_MOESM3_ESM.docx

Extended discussion: Potential events occurring during bud dormancy release as reflected by the nature of regulation of individual genes within different functional categories and their role in other biological systems. (DOCX 30 kb)

Gene annotation and clone to gene grouping. (XLS 2269 kb)

11103_2009_9531_MOESM5_ESM.pdf

Fig. S1 Validation of the effect of HC and HS application on transcript level of selected genes in grape buds by northern analysis. Northern-blot analyses were conducted as described in Fig. 8. Blots were probed with radiolabeled PCR products amplified from clones representing the following ESTs: ADH (TC27342); PDC (TC33368); CAT (TC25121); APX (TC45171); SuSy (TC31786); Trxh (TC 25169); GST (NP864091); ABC (TC32869); StSy (TC35597); CaM (TC339147) CaATP ( TC35289) and CBP (TC 34227). (PDF 1052 kb)

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Ophir, R., Pang, X., Halaly, T. et al. Gene-expression profiling of grape bud response to two alternative dormancy-release stimuli expose possible links between impaired mitochondrial activity, hypoxia, ethylene-ABA interplay and cell enlargement. Plant Mol Biol 71, 403 (2009). https://doi.org/10.1007/s11103-009-9531-9

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