Advertisement

Plant Molecular Biology

, Volume 98, Issue 6, pp 507–523 | Cite as

Transient induction of a subset of ethylene biosynthesis genes is potentially involved in regulation of grapevine bud dormancy release

  • Zhaowan Shi
  • Tamar Halaly-Basha
  • Chuanlin Zheng
  • Mira Weissberg
  • Ron Ophir
  • David W. Galbraith
  • Xuequn Pang
  • Etti Or
Article

Abstract

Key message

Transient increases in ethylene biosynthesis, achieved by tight regulation of transcription of specific ACC oxidase and ACC synthase genes, play a role in activation of grapevine bud dormancy release.

Abstract

The molecular mechanisms regulating dormancy release in grapevine buds are as yet unclear. It has been hypothesized that its core involves perturbation of respiration which induces an interplay between ethylene and ABA metabolism that removes repression and allows regrowth. Roles for hypoxia and ABA metabolism in this process have been previously supported. The potential involvement of ethylene biosynthesis in regulation of dormancy release, which has received little attention so far, is now explored. Our results indicate that (1) ethylene biosynthesis is induced by hydrogen cyanamide (HC) and azide (AZ), known artificial stimuli of dormancy release, (2) inhibitors of ethylene biosynthesis and signalling antagonize dormancy release by HC/AZ treatments, (3) ethylene application induces dormancy release, (4) there are two sets of bud-expressed ethylene biosynthesis genes which are differentially regulated, (5) only one set is transiently upregulated by HC/AZ and during the natural dormancy cycle, concomitant with changes in ethylene levels, and (6) levels of ACC oxidase transcripts and ethylene sharply decrease during natural dormancy release, whereas ACC accumulates. Given these results, we propose that transient increases in ethylene biosynthesis prior to dormancy release, achieved primarily by regulation of transcription of specific ACC oxidase genes, play a role in activation of dormancy release.

Keywords

Vitis vinifera ACC synthase (ACS) ACC oxidase (ACO) Bud Dormancy Ethylene Grapevine 

Notes

Acknowledgements

This research was supported by the United States-Israel Binational Agricultural Research and Development Fund (BARD Grant No. IS-4639-13 to EO, DG, and RO). We thank Felix Shaya from the metabolomics unit of ARO for ACC quantitation. We also thank the China Scholarship Council for joint PhD fellowships provided to Zhaowan Shi.

Author contributions

Conceptualization: ZS, TH-B, RO, DWG, EO; investigation: ZS, TH-B, CZ, MW; writing—original draft: ZS, TH-B, EO; writing—review & editing: RO, DWG, XP, EO.

Supplementary material

11103_2018_793_MOESM1_ESM.pptx (883 kb)
Supplementary material 1 (PPTX 883 KB)
11103_2018_793_MOESM2_ESM.xls (396 kb)
Supplementary material 2 (XLS 396 KB)

References

  1. Acheampong AK, Zheng C, Halaly T, Giacomelli L, Takebayashi Y, Jikumaru Y, Kamiya Y, Lichter A, Or E (2017) Abnormal endogenous repression of GA signaling in a seedless table grape cultivar with high berry growth response to GA application. Front Plant Sci 8:850.  https://doi.org/10.3389/fpls.2017.00850 CrossRefGoogle Scholar
  2. Aksenova NP, Sergeeva LI, Konstantinova TN, Golyanovskaya SA, Kolachevskaya OO, Romanov GA (2013) Regulation of potato tuber dormancy and sprouting. Russ J Plant Physiol 60:301–312.  https://doi.org/10.1134/S1021443713030023 CrossRefGoogle Scholar
  3. Alexopoulos AA, Aivalakis G, Akoumianakis KA, Passam HC (2009) Bromoethane induces dormancy breakage and metabolic changes in tubers derived from true potato seed. Postharvest Biol Technol 54:165–171.  https://doi.org/10.1016/j.postharvbio.2009.07.004 CrossRefGoogle Scholar
  4. Beyer EM (1976) A potent inhibitor of ethylene action in plants. Plant Physiol 58:268–271.  https://doi.org/10.1104/pp.58.3.268 CrossRefGoogle Scholar
  5. Carrera E, Holman T, Medhurst A, Dietrich D, Footitt S, Theodoulou FL, Holdsworth MJ (2008) Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. Plant J 53:214–224.  https://doi.org/10.1111/j.1365-313X.2007.03331.x CrossRefGoogle Scholar
  6. Chao WS, Doğramacı M, Horvath DP, Anderson JV, Foley ME (2017) Comparison of phytohormone levels and transcript profiles during seasonal dormancy transitions in underground adventitious buds of leafy spurge. Plant Mol Biol 94:281–302.  https://doi.org/10.1007/s11103-017-0607-7 CrossRefGoogle Scholar
  7. Cheng W-H, Chiang M-H, Hwang S-G, Lin P-C (2009) Antagonism between abscisic acid and ethylene in Arabidopsis acts in parallel with the reciprocal regulation of their metabolism and signaling pathways. Plant Mol Biol 71:61–80.  https://doi.org/10.1007/s11103-009-9509-7 CrossRefGoogle Scholar
  8. Cheng Y, Liu J, Yang X, Ma R, Liu Q, Liu C (2013) Construction of ethylene regulatory network based on the phytohormones related gene transcriptome profiling and prediction of transcription factor activities in soybean. Acta Physiol Plant 35:1303–1317.  https://doi.org/10.1007/s11738-012-1170-0 CrossRefGoogle Scholar
  9. Corbineau F, Xia Q, Bailly C, El-Maarouf-Bouteau H (2014) Ethylene, a key factor in the regulation of seed dormancy. Front Plant Sci 5:539.  https://doi.org/10.3389/fpls.2014.00539 CrossRefGoogle Scholar
  10. Dal Ri A, Pilati S, Velasco R, Moser C, Costa G, Boschetti A (2009) Ethylene production during grape berry development and expression of genes involved in ethylene biosynthesis and response. In: XI international symposium on plant bioregulators in fruit production, vol 884, pp 73–80.  https://doi.org/10.17660/ActaHortic.2010.884.6
  11. Dekel Y, Machluf Y, Ben-Dor S, Yifa O, Stoler A, Ben-Shlomo I, Bercovich D (2015) Dispersal of an ancient retroposon in the TP53 promoter of Bovidae: phylogeny, novel mechanisms, and potential implications for cow milk persistency. BMC Genomics 16:53.  https://doi.org/10.1186/s12864-015-1235-8 CrossRefGoogle Scholar
  12. Doğramacı M, Foley ME, Chao WS, Christoffers MJ, Anderson JV (2013) Induction of endodormancy in crown buds of leafy spurge (Euphorbia esula L.) implicates a role for ethylene and cross-talk between photoperiod and temperature. Plant Mol Biol 81:577–593.  https://doi.org/10.1007/s11103-013-0026-3 CrossRefGoogle Scholar
  13. Fasoli M, Dal Santo S, Zenoni S, Tornielli GB, Farina L, Zamboni A, Porceddu A, Venturini L, Bicego M, Murino V (2012) The grapevine expression atlas reveals a deep transcriptome shift driving the entire plant into a maturation program. Plant Cell 24:3489–3505.  https://doi.org/10.1105/tpc.112.100230 CrossRefGoogle Scholar
  14. Fennell AY, Schlauch KA, Gouthu S, Deluc LG, Khadka V, Sreekantan L, Grimplet J, Cramer GR, Mathiason KL (2015) Short day transcriptomic programming during induction of dormancy in grapevine. Front Plant Sci 6:834.  https://doi.org/10.3389/fpls.2015.00834 CrossRefGoogle Scholar
  15. Fukao T, Bailey-Serres J (2008) Ethylene—a key regulator of submergence responses in rice. Plant Sci 175:43–51.  https://doi.org/10.1016/j.plantsci.2007.12.002 CrossRefGoogle Scholar
  16. Harpaz-Saad S, Yoon GM, Mattoo AK, Kieber JJ (2012) The formation of ACC and competition between polyamines and ethylene for SAM. In: McManus MT (ed) Annual plant reviews volume 44: the plant hormone ethylene. Hoboken, Blackwell Publishing Ltd, pp 53–81.  https://doi.org/10.1002/9781118223086.ch3 CrossRefGoogle Scholar
  17. Hartmann A, Senning M, Hedden P, Sonnewald U, Sonnewald S (2011) Reactivation of meristem activity and sprout growth in potato tubers require both cytokinin and gibberellin. Plant Physiol 155:776–796.  https://doi.org/10.1104/pp.110.168252 CrossRefGoogle Scholar
  18. Hoffmann-Benning S, Kende H (1992) On the role of abscisic acid and gibberellin in the regulation of growth in rice. Plant Physiol 99:1156–1161.  https://doi.org/10.1104/pp.99.3.1156 CrossRefGoogle Scholar
  19. Höfler S, Lorenz C, Busch T, Brinkkötter M, Tohge T, Fernie AR, Braun HP, Hildebrandt TM (2016) Dealing with the sulfur part of cysteine: four enzymatic steps degrade l-cysteine to pyruvate and thiosulfate in Arabidopsis mitochondria. Physiol Plant 157:352–366.  https://doi.org/10.1111/ppl.12454 CrossRefGoogle Scholar
  20. Horvath DP, Chao WS, Suttle JC, Thimmapuram J, Anderson JV (2008) Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions of leafy spurge (Euphorbia esula L.). BMC Genomics 9:536.  https://doi.org/10.1186/1471-2164-9-536 CrossRefGoogle Scholar
  21. Howe GT, Horvath DP, Dharmawardhana P, Priest HD, Mockler TC, Strauss SH (2015) Extensive transcriptome changes during natural onset and release of vegetative bud dormancy in Populus. Front Plant Sci 6:989.  https://doi.org/10.3389/fpls.2015.00989 CrossRefGoogle Scholar
  22. Ibraheem O, Botha CE, Bradley G (2010) In silico analysis of cis-acting regulatory elements in 5′ regulatory regions of sucrose transporter gene families in rice (Oryza sativa Japonica) and Arabidopsis thaliana. Comput Biol Chem 34:268–283.  https://doi.org/10.1016/j.compbiolchem.2010.09.003 CrossRefGoogle Scholar
  23. Ionescu IA, López-Ortega G, Burow M, Bayo-Canha A, Junge A, Gericke O, Møller BL, Sánchez-Pérez R (2017) Transcriptome and metabolite changes during hydrogen cyanamide-induced floral bud break in sweet cherry. Front Plant Sci 8:1233.  https://doi.org/10.3389/fpls.2017.01233 CrossRefGoogle Scholar
  24. Iwai T, Miyasaka A, Seo S, Ohashi Y (2006) Contribution of ethylene biosynthesis for resistance to blast fungus infection in young rice plants. Plant Physiol 142:1202–1215.  https://doi.org/10.1104/pp.106.085258 CrossRefGoogle Scholar
  25. Khalil-Ur-Rehman M, Sun L, Li C-X, Faheem M, Wang W, Tao J-M (2017) Comparative RNA-seq based transcriptomic analysis of bud dormancy in grape. BMC Plant Biol 17:18.  https://doi.org/10.1186/s12870-016-0960-8 CrossRefGoogle Scholar
  26. Konishi M, Yanagisawa S (2010) Identification of a nitrate-responsive cis-element in the Arabidopsis NIR1 promoter defines the presence of multiple cis-regulatory elements for nitrogen response. Plant J 63:269–282.  https://doi.org/10.1111/j.1365-313X.2010.04239.x CrossRefGoogle Scholar
  27. Kumar G, Gupta K, Pathania S, Swarnkar MK, Rattan UK, Singh G, Sharma RK, Singh AK (2017) Chilling affects phytohormone and post-embryonic development pathways during bud break and fruit set in apple (Malus domestica Borkh.). Sci Rep 7:42593.  https://doi.org/10.1111/j.1365-313X.2010.04239.x CrossRefGoogle Scholar
  28. Linkies A, Leubner-Metzger G (2012) Beyond gibberellins and abscisic acid: how ethylene and jasmonates control seed germination. Plant Cell Rep 31:253–270.  https://doi.org/10.1007/s00299-011-1180-1 CrossRefGoogle Scholar
  29. Linkies A, Müller K, Morris K, Turečková V, Wenk M, Cadman CS, Corbineau F, Strnad M, Lynn JR, Finch-Savage WE (2009) Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell 21:3803–3822.  https://doi.org/10.1105/tpc.109.070201 CrossRefGoogle Scholar
  30. Liu M, Pirrello J, Chervin C, Roustan J-P, Bouzayen M (2015) Ethylene control of fruit ripening: revisiting the complex network of transcriptional regulation. Plant Physiol 169:2380–2390.  https://doi.org/10.1104/pp.15.01361 CrossRefGoogle Scholar
  31. Meitha K, Agudelo-Romero P, Signorelli S, Gibbs DJ, Considine JA, Foyer CH, Considine MJ (2018) Developmental control of hypoxia during bud burst in grapevine. Plant Cell Environ 41(5):1154–1170.  https://doi.org/10.1111/pce.13141 CrossRefGoogle Scholar
  32. Merritt F, Kemper A, Tallman G (2001) Inhibitors of ethylene synthesis inhibit auxin-induced stomatal opening in epidermis detached from leaves of Vicia faba L. Plant Cell Physiol 42:223–230.  https://doi.org/10.1093/pcp/pce030 CrossRefGoogle Scholar
  33. Müller M, Munné-Bosch S (2011) Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Plant Methods 7:37.  https://doi.org/10.1186/1746-4811-7-37 CrossRefGoogle Scholar
  34. Muñoz-Robredo P, Gudenschwager O, Chervin C, Campos-Vargas R, González-Agüero M, Defilippi BG (2013) Study on differential expression of 1-aminocyclopropane-1-carboxylic acid oxidase genes in table grape cv Thompson seedless. Postharvest Biol Technol 76:163–169.  https://doi.org/10.1016/j.postharvbio.2012.10.006 CrossRefGoogle Scholar
  35. Narsai R, Law SR, Carrie C, Xu L, Whelan J (2011) In-depth temporal transcriptome profiling reveals a crucial developmental switch with roles for RNA processing and organelle metabolism that are essential for germination in Arabidopsis. Plant Physiol 157:1342–1362.  https://doi.org/10.1104/pp.111.183129 CrossRefGoogle Scholar
  36. Ophir R, Pang X, Halaly T, Venkateswari J, Lavee S, Galbraith D, Or E (2009) 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.  https://doi.org/10.1007/s11103-009-9531-9 CrossRefGoogle Scholar
  37. Penfield S, Li Y, Gilday AD, Graham S, Graham IA (2006) Arabidopsis ABA INSENSITIVE4 regulates lipid mobilization in the embryo and reveals repression of seed germination by the endosperm. Plant Cell 18:1887–1899.  https://doi.org/10.1105/tpc.106.041277 CrossRefGoogle Scholar
  38. Peng H-P, Lin T-Y, Wang N-N, Shih M-C (2005) Differential expression of genes encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis during hypoxia. Plant Mol Biol 58:15–25.  https://doi.org/10.1007/s11103-005-3573-4 CrossRefGoogle Scholar
  39. Prange RK, Kalt W, Daniels-Lake BJ, Liew CL, Page RT, Walsh JR, Dean P, Coffin R (1998) Using ethylene as a sprout control agent in stored ‘Russet Burbank’ potatoes. J Am Soc Hortic Sci 123:463–469Google Scholar
  40. Ruonala R, Rinne PL, 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.  https://doi.org/10.1111/j.1365-313X.2006.02722.x CrossRefGoogle Scholar
  41. Ruttink T, Arend M, Morreel K, Storme V, Rombauts S, Fromm J, Bhalerao RP, Boerjan W, Rohde A (2007) A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19:2370–2390.  https://doi.org/10.1105/tpc.107.052811 CrossRefGoogle Scholar
  42. Rylski I, Rappaport L, Pratt HK (1974) Dual effects of ethylene on potato dormancy and sprout growth. Plant Physiol 53:658–662.  https://doi.org/10.1104/pp.53.4.658 CrossRefGoogle Scholar
  43. Saika H, Okamoto M, Miyoshi K, Kushiro T, Shinoda S, Jikumaru Y, Fujimoto M, Arikawa T, Takahashi H, Ando M (2007) Ethylene promotes submergence-induced expression of OsABA8ox1, a gene that encodes ABA 8′-hydroxylase in rice. Plant Cell Physiol 48:287–298.  https://doi.org/10.1093/pcp/pcm003 CrossRefGoogle Scholar
  44. Sonnewald S, Sonnewald U (2014) Regulation of potato tuber sprouting. Planta 239:27–38.  https://doi.org/10.1007/s00425-013-1968-z CrossRefGoogle Scholar
  45. Sudawan B, Chang C-S, Chao H-f, Ku MS, Yen Y-f (2016) Hydrogen cyanamide breaks grapevine bud dormancy in the summer through transient activation of gene expression and accumulation of reactive oxygen and nitrogen species. BMC Plant Biol 16:202.  https://doi.org/10.1186/s12870-016-0889-y CrossRefGoogle Scholar
  46. Sumitomo K, Narumi T, Satoh S, Hisamatsu T (2008) Involvement of the ethylene response pathway in dormancy induction in chrysanthemum. J Exp Bot 59:4075–4082.  https://doi.org/10.1093/jxb/ern247 CrossRefGoogle Scholar
  47. Suttle JC (1998) Involvement of ethylene in potato microtuber dormancy. Plant Physiol 118:843–848.  https://doi.org/10.1104/pp.118.3.843 CrossRefGoogle Scholar
  48. Suttle JC (2009) Ethylene is not involved in hormone- and bromoethane-induced dormancy break in Russet Burbank minitubers. Am J Potato Res 86:278–285.  https://doi.org/10.1007/s12230-009-9081-3 CrossRefGoogle Scholar
  49. Tarancón C, González-Grandío E, Oliveros JC, Nicolas M, Cubas P (2017) A conserved carbon starvation response underlies bud dormancy in woody and Herbaceous species. Front Plant Sci 8:788.  https://doi.org/10.3389/fpls.2017.00788 CrossRefGoogle Scholar
  50. Tsuchisaka A, Theologis A (2004) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol 136:2982–3000.  https://doi.org/10.1104/pp.104.049999 CrossRefGoogle Scholar
  51. Tsuchisaka A, Yu G, Jin H, Alonso JM, Ecker JR, Zhang X, Gao S, Theologis A (2009) A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics 183:979–1003.  https://doi.org/10.1534/genetics.109.107102 CrossRefGoogle Scholar
  52. Tsukaya H, Ohshima T, Naito S, Chino M, Komeda Y (1991) Sugar-dependent expression of the CHS-A gene for chalcone synthase from petunia in transgenic Arabidopsis. Plant Physiol 97:1414–1421.  https://doi.org/10.1104/pp.97.4.1414 CrossRefGoogle Scholar
  53. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971.  https://doi.org/10.1105/tpc.9.11.1963 CrossRefGoogle Scholar
  54. Upadhyay RK, Gupta A, Soni D, Garg R, Pathre UV, Nath P, Sane AP (2017) Ectopic expression of a tomato DREB gene affects several ABA processes and influences plant growth and root architecture in an age-dependent manner. J Plant Physiol 214:97–107.  https://doi.org/10.1016/j.jplph.2017.04.004 CrossRefGoogle Scholar
  55. Van de Poel B, Van Der Straeten D (2014) 1-aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene! Front Plant Sci 5:640.  https://doi.org/10.3389/fpls.2014.00640_ CrossRefGoogle Scholar
  56. Vanderstraeten L, Van Der Straeten D (2017) Accumulation and transport of 1-aminocyclopropane-1-carboxylic acid (ACC) in plants: current status, considerations for future research and agronomic applications. Front Plant Sci 8:38.  https://doi.org/10.3389/fpls.2017.00038 CrossRefGoogle Scholar
  57. Vergara R, Noriega X, Aravena K, Prieto H, Pérez FJ (2017) ABA represses the expression of cell cycle genes and may modulate the development of endodormancy in grapevine buds. Front Plant Sci 8:812.  https://doi.org/10.3389/fpls.2017.00812 CrossRefGoogle Scholar
  58. Xia Q, Saux M, Ponnaiah M, Gilard F, Perreau F, Huguet S, Balzergue S, Langlade N, Bailly C, Meimoun P et al (2018) One way to achieve germination: common molecular mechanism induced by ethylene and after-ripening in sunflower seeds. Int J Mol Sci 19:2464.  https://doi.org/10.3390/ijms19082464 CrossRefGoogle Scholar
  59. Xu M, Wang M-H (2012) Genome-wide analysis of 1-amino-cyclopropane-1-carboxylate synthase gene family in Arabidopsis, rice, grapevine and poplar. Afr J Biotechnol 11:1106–1118.  https://doi.org/10.5897/AJB11.773 CrossRefGoogle Scholar
  60. Yant L, Mathieu J, Dinh TT, Ott F, Lanz C, Wollmann H, Chen X, Schmid M (2010) Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 22:2156–2170.  https://doi.org/10.1105/tpc.110.075606 CrossRefGoogle Scholar
  61. Yoon GM (2015) New insights into the protein turnover regulation in ethylene biosynthesis. Mol Cells 38:597–603.  https://doi.org/10.14348/molcells.2015.0152 CrossRefGoogle Scholar
  62. Yordanov YS, Ma C, Strauss SH, Busov VB (2014) EARLY BUD-BREAK 1 (EBB1) is a regulator of release from seasonal dormancy in poplar trees. Proc Natl Acad Sci USA 111:10001–10006.  https://doi.org/10.1073/pnas.1405621111 CrossRefGoogle Scholar
  63. Zheng C, Halaly T, Acheampong AK, Takebayashi Y, Jikumaru Y, Kamiya Y, Or E (2015) Abscisic acid (ABA) regulates grape bud dormancy, and dormancy release stimuli may act through modification of ABA metabolism. J Exp Bot 66:1527–1542.  https://doi.org/10.1093/jxb/eru519 CrossRefGoogle Scholar
  64. Zheng C, Acheampong AK, Shi Z, Halaly T, Kamiya Y, Ophir R, Galbraith DW, Or E (2018) Distinct gibberellin functions during and after grapevine bud dormancy release. J Exp Bot 69(7):1635–1648.  https://doi.org/10.1093/jxb/ery022 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Zhaowan Shi
    • 1
    • 2
  • Tamar Halaly-Basha
    • 1
  • Chuanlin Zheng
    • 1
  • Mira Weissberg
    • 1
  • Ron Ophir
    • 1
  • David W. Galbraith
    • 3
  • Xuequn Pang
    • 2
  • Etti Or
    • 1
  1. 1.Institute of Plant Sciences, Department of Fruit Tree Sciences, Agricultural Research OrganizationVolcani CenterRishon LeZionIsrael
  2. 2.College of Life SciencesSouth China Agricultural UniversityGuangzhouChina
  3. 3.School of Plant Sciences and Bio5 InstituteUniversity of ArizonaTucsonUSA

Personalised recommendations