Plant Molecular Biology

, 71:403 | Cite as

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

  • Ron Ophir
  • Xuequn Pang
  • Tamar Halaly
  • Jaganatha Venkateswari
  • Shimon Lavee
  • David Galbraith
  • Etti Or


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.


Bud Hypoxia Grapevine Dormancy release Ethylene 

Supplementary material

11103_2009_9531_MOESM1_ESM.xls (6.3 mb)
Description of clone-to-gene analysis and content of file S2 and S3. (XLS 6436 kb)
11103_2009_9531_MOESM2_ESM.doc (69 kb)
Clones differential expression analysis results. (DOC 69 kb)
11103_2009_9531_MOESM3_ESM.docx (29 kb)
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)
11103_2009_9531_MOESM4_ESM.xls (2.2 mb)
Gene annotation and clone to gene grouping. (XLS 2269 kb)
11103_2009_9531_MOESM5_ESM.pdf (1 mb)
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)


  1. Baud S, Vaultier MN, Rochat C (2004) Structure and expression of the sucrose synthase multigene family in Arabidopsis. J Exp Bot 396:397–409CrossRefGoogle Scholar
  2. 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 143:312–325CrossRefPubMedGoogle Scholar
  3. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B Met 57:289–300Google Scholar
  4. 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 44:756–768CrossRefPubMedGoogle Scholar
  5. 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 141:1644–1652CrossRefPubMedGoogle Scholar
  6. Beveridge CA, Mathesius U, Rose RJ, Gresshoff PM (2007) Common regulatory themes in meristem development and whole-plant homeostasis. Curr Opin Plant Biol 10:44–51CrossRefPubMedGoogle Scholar
  7. Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, RockvilleGoogle Scholar
  8. 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 165:662–670CrossRefPubMedGoogle Scholar
  9. 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 1757:730–741CrossRefPubMedGoogle Scholar
  10. 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 136:2948–2960CrossRefPubMedGoogle Scholar
  11. Crawford RMM (1977) Tolerance of anoxia and ethanol metabolism in germinating seeds. New Phytol 79:511–517CrossRefGoogle Scholar
  12. Dokoozlian NK (1999) Chilling temperature and duration interact on the bud break of ‘perlette’ grapevine cuttings. HortScience 34:1054–1056Google Scholar
  13. Dokoozlian NZ, Williams Wang LE, Neja RA (1995) Chilling exposure and hydrogen cyanamide interact in breaking dormancy of grape buds. HortScience 30:1244–1247Google Scholar
  14. 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 1:34–37CrossRefGoogle Scholar
  15. Erez A (1987) Chemical control of bud break. HortScience 22:1240–1243Google Scholar
  16. Erez A (1995) Means to compensate for insufficient chilling to improve bloom and leafing. Acta Hort 395:81–95Google Scholar
  17. 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 69–78Google Scholar
  18. 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 32:623–628Google Scholar
  19. 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:R80CrossRefPubMedGoogle Scholar
  20. George AP, Nissen RJ, Baker JA (1986) Low chill peach and nectarine cultivars. Qld Agric J 112:27–33Google Scholar
  21. 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 12:1117–1126CrossRefPubMedGoogle Scholar
  22. 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 24:265–276PubMedGoogle Scholar
  23. 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 45:955–967CrossRefPubMedGoogle Scholar
  24. 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 228:79–88CrossRefPubMedGoogle Scholar
  25. 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 273:26857–26861CrossRefPubMedGoogle Scholar
  26. 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 8:311–321CrossRefPubMedGoogle Scholar
  27. Horvath DP, Chao WS, Anderson JV (2002) Molecular analysis of signals controlling dormancy and growth in underground adventitious buds of leafy spurge. Plant Physiol 128:1439–1446CrossRefPubMedGoogle Scholar
  28. 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–S104PubMedGoogle Scholar
  29. Igamberdiev AU, Seregelyes C, Manach N, Hill RD (2004) NADH-dependent metabolism of nitric oxide in alfalfa root cultures expressing barley hemoglobin. Planta 219:95–102CrossRefPubMedGoogle Scholar
  30. 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 48:395–398CrossRefGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. 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 61:255–268CrossRefPubMedGoogle Scholar
  33. 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 173:446–457CrossRefGoogle Scholar
  34. Kende H, van der Knaap E, Cho HT (1998) Deepwater rice: a model plant to study stem elongation. Plant Physiol 118:1105–1110CrossRefPubMedGoogle Scholar
  35. Klingenberg M (1989) Molecular aspects of adenine nucleotide carrier from mitochondria. Arch Biochem Biophys 270:1–14CrossRefPubMedGoogle Scholar
  36. Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246CrossRefPubMedGoogle Scholar
  37. 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 33:63–67Google Scholar
  38. 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 149:461–473CrossRefPubMedGoogle Scholar
  39. Lang GA (1987) Dormancy: a new universal terminology. HortScience 22:817–820Google Scholar
  40. 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 144:218–231CrossRefPubMedGoogle Scholar
  41. Lavee S, May P (1997) Dormancy of grapevine buds. Aust J Grape Wine Res 3:31–46CrossRefGoogle Scholar
  42. Liotenberg S, North H, Marion-Poll A (1999) Molecular biology and regulation of abscisic acid biosynthesis in plants. Plant Physiol Biochem 37:341–350CrossRefGoogle Scholar
  43. 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 137:1115–1129CrossRefPubMedGoogle Scholar
  44. 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 88:167–172CrossRefPubMedGoogle Scholar
  45. 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: 18633655Google Scholar
  46. 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 58:1035–1045CrossRefPubMedGoogle Scholar
  47. Métraux JP, Kende H (1983) The role of ethylene in the growth response of submerged deepwater rice. Plant Physiol 72:441–446CrossRefPubMedGoogle Scholar
  48. 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 91–97Google Scholar
  49. 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 52:561–591CrossRefPubMedGoogle Scholar
  50. Nie X, Hill RD (1997) Mitochondrial respiration and hemoglobin gene expression in barley aleurone tissue. Plant Physiol 114:835–840PubMedGoogle Scholar
  51. Nir G, Lavee S (1993) Metabolic changes during cyanimide induced dormancy release in grapevines. Acta Hort 329:271–274Google Scholar
  52. Nir G, Shulman Y, Fanberstein L, Lavee S (1986) Changes in the activity of catalase (EC in relation to the dormancy of grapevine (Vitis vinifera L.) buds. Plant Physiol 81:1140–1142CrossRefPubMedGoogle Scholar
  53. Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182CrossRefPubMedGoogle Scholar
  54. Olsen JE (2003) Molecular and physiological mechanisms of bud dormancy regulation. Acta Hort 618:437–453Google Scholar
  55. Or E, Nir G, Vilozny I (1999) Timing of hydrogen cyanamide application to grapevine buds. Vitis 38:1–6Google Scholar
  56. 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 75:190–194Google Scholar
  57. 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 43:483–489CrossRefPubMedGoogle Scholar
  58. 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 162:121–130CrossRefGoogle Scholar
  59. 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 59:2241–2251CrossRefPubMedGoogle Scholar
  60. 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)Google Scholar
  61. 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 3:144–152CrossRefPubMedGoogle Scholar
  62. 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 58:3249–3262CrossRefPubMedGoogle Scholar
  63. Patel M, Day BJ, Crapo JD, Fridovich I, McNamara JO (1996) Requirement for superoxide in excitotoxic cell death. Neuron 16:345–355CrossRefPubMedGoogle Scholar
  64. 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 53:391–398CrossRefPubMedGoogle Scholar
  65. Perez FJ, Lira W (2005) Possible role of catalase in post-dormancy bud break in grapevines. J Plant Physiol 162:301–308CrossRefPubMedGoogle Scholar
  66. 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 34:624–632CrossRefGoogle Scholar
  67. Perez FJ, Vergara S, Rubio S (2008) H2O2 is involved in the dormancy-breaking effect of hydrogen cyanamide in grapevine buds. Plant Growth Regul 55:149–155CrossRefGoogle Scholar
  68. Pesis E, Marinansky R, Zauberman G, Fuchs Y (1994) Prestorage low-oxygen atmosphere treatment reduces chilling injury symptoms in Fuerte avocado fruit. HortScience 29:1042–1046Google Scholar
  69. 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 47:1195–1205CrossRefPubMedGoogle Scholar
  70. Rehling P, Pfanner N, Meisinger C (2003) Insertion of hydrophobic membrane proteins into the inner mitochondrial membrane—a guided tour. J Mol Biol 326:639–657CrossRefPubMedGoogle Scholar
  71. 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 57:3079–3089CrossRefPubMedGoogle Scholar
  72. 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 46:628–640CrossRefPubMedGoogle Scholar
  73. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  74. Saure M (1985) Dormancy release in deciduous fruit trees. Hort Rev 7:239–300Google Scholar
  75. 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 40:173–187CrossRefPubMedGoogle Scholar
  76. 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 174:5057–5062PubMedGoogle Scholar
  77. Shulman Y, Nir G, Fanberstein L, Lavee S (1983) The effect of cyanamide on the release from dormancy of grapevine buds. Sci Hort 19:97–104CrossRefGoogle Scholar
  78. Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Gen Mol Biol 3: article 3Google Scholar
  79. 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, BruxellesGoogle Scholar
  80. Smyth GK, Michaud J, Scott HS (2005) Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21:2067–2075CrossRefPubMedGoogle Scholar
  81. 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 12:3703–3714CrossRefPubMedGoogle Scholar
  82. 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 17:2384–2396CrossRefPubMedGoogle Scholar
  83. 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 223:604–612CrossRefPubMedGoogle Scholar
  84. Subbaiah CC, Sachs MM (2003) Molecular and cellular adaptations of maize to flooding stress. Ann Bot 91:119–127CrossRefPubMedGoogle Scholar
  85. Sun T, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55:197–223CrossRefPubMedGoogle Scholar
  86. Suttle JC (1998) Postharvest changes in endogenous cytokinins and cytokinin efficacy in potato tubers in relation to bud endodormancy. Physiol Plant 103:59–69CrossRefGoogle Scholar
  87. 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 32:891–904CrossRefPubMedGoogle Scholar
  88. 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 71:504–515CrossRefPubMedGoogle Scholar
  89. 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 24:853–862CrossRefPubMedGoogle Scholar
  90. 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 67:897–901CrossRefGoogle Scholar
  91. 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 550:149–154CrossRefPubMedGoogle Scholar
  92. 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 103:783–791PubMedGoogle Scholar
  93. Wang SY, Jiao HJ, Faust M (1991a) Changes in ascorbate, glutathione, and related enzyme activities during thidiazuron-induced bud break of apple. Physiol Plant 82:231–236CrossRefGoogle Scholar
  94. Wang SY, Jiao HJ, Faust M (1991b) Changes in metabolic enzyme activities during thidiazuron-induced lateral budbreak of apple. HortScience 82:231–236Google Scholar
  95. 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:e15CrossRefPubMedGoogle Scholar
  96. 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 18:589–600CrossRefPubMedGoogle Scholar
  97. 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 19:3037–3057CrossRefPubMedGoogle Scholar
  98. 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 220:262–270CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Ron Ophir
    • 1
  • Xuequn Pang
    • 1
    • 2
  • Tamar Halaly
    • 1
  • Jaganatha Venkateswari
    • 3
    • 4
  • Shimon Lavee
    • 1
  • David Galbraith
    • 3
  • Etti Or
    • 1
  1. 1.Department of Fruit Tree Sciences, Institute of Horticulture, Agricultural Research OrganizationThe Volcani CenterBet DaganIsrael
  2. 2.College of Life ScienceSouth China Agricultural UniversityGuangzhouChina
  3. 3.Department of Plant Sciences and Bios InstituteUniversity of ArizonaTucsonUSA
  4. 4.Department of Botany and Plant Sciences, 2150 Batchelor HallUniversity of CaliforniaRiversideUSA

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