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Horticulture, Environment, and Biotechnology

, Volume 58, Issue 6, pp 568–575 | Cite as

Pre-bloom application of gibberellin in ‘Tamnara’ grape increases γ-aminobutyric acid (GABA) production at full bloom

  • Chan Jin Jung
  • Youn Young Hur
  • Jin Seok Moon
  • Sung-Min Jung
Research Report

Abstract

A pre-bloom application of gibberellin (GA) on grapevines (Vitis spp.) induces fruit set without fertilization (parthenocarpy) by inhibiting pollen tube growth. In the present study, we analyzed transcriptional changes in the Vitis γ-aminobutyric acid (GABA) metabolic genes and the levels of GABA in grapevines with or without GA treatment to understand how GA induces parthenocarpy in grapevines. Four Vitis glutamate decarboxylases (VvGAD), two GABA transaminases (VvGABA-T), and three succinic semialdehyde dehydrogenases (VvSSADH) were identified in grapevines, and their expression patterns were analyzed during inflorescence development from 14 days before full bloom (DBF) to 5 days after full bloom (DAF). Without GA treatment, we observed simultaneously high expression levels of VvGAD1 and VvGABA-T2, with low levels of GABA from 10 to 5 DBF. With GA application, the levels of GABA were mostly unaltered, and the expression levels of VvGAD1 and VvGABA-T2 were around 30% lower compared to the plants without GA treatment at 12 DBF. However, at near full bloom in the plants treated with GA, GABA levels increased more than two-fold and VvGAD1 was upregulated. These results indicate that GABA levels are tightly regulated by VvGAD1 and VvGABA-T2 before pollination and that application of GA alters the pattern of GABA accumulation at near full bloom. This is the first report to describe how treatment with GA disrupts the crosstalk between the pistil and pollen via changes in GABA metabolism during GA-mediated parthenocarpic fruit initiation.

Additional key words

GABA glutamate decarboxylase succinic semialdehyde dehydrogenase γ-aminobutyric acid transaminase 

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Supplementary material

13580_2017_62_MOESM1_ESM.xlsx (1.5 mb)
Supplementary Fig. 1. Comparison of Vitis GABA metabolic enzymes with those in Arabidopsis and tomato.

References

  1. Akihiro T, Koike S, Tani R, Tominaga T, Watanabe S, Iijima Y, Aoki K, Shibata D, Ashihara H et al (2008) Biochemical mechanism on GABA accumulation during fruit development in tomato. Plant Cell Physiol 49:1378–1389CrossRefPubMedGoogle Scholar
  2. Baum G, Lev-Yadun S, Fridmann Y, Arazi T, Katsnelson H, Zik M, Fromm H (1996) Calmodulin binding to glutamate decarboxylase is required for regulation of glutamate and GABA metabolism and normal development in plants. EMBO J 15:2988–2996PubMedPubMedCentralCrossRefGoogle Scholar
  3. Biancucci M, Mattioli R, Forlani G, Funck D, Costantino P, Trovato M (2015) Role of proline and GABA in sexual reproduction of angiosperms. Front Plant Sci 6:680CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bolarín MC, Santa-Cruz A, Cayuela E, Pérez-Alfocea F (1995) Short-term solute changes in leaves and roots of cultivated and wild tomato seedlings under salinity. J Plant Physiol 147:463–468CrossRefGoogle Scholar
  5. Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115CrossRefPubMedGoogle Scholar
  6. Carrera E, Ruiz-Rivero O, Peres LEP, Atares A, Garcia-Martinez JL (2012) Characterization of the procera tomato mutant shows novel functions of the SlDELLA protein in the control of flower morphology, cell division and expansion, and the auxin-signaling pathway during fruit-set and development. Plant Physiol 160:1581–96CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116CrossRefGoogle Scholar
  8. Coombe BG (1960) Relationship of growth and development to changes in sugars, auxins, and gibberellins in fruit of seeded and seedless varieties of Vitis vinifera. Plant Physiol 35:241–50CrossRefPubMedPubMedCentralGoogle Scholar
  9. Coombe BG (1995) Adoption of a system for identifying grapevine growth stages. Aust J Grape Wine Res 1:100–110CrossRefGoogle Scholar
  10. Dass HC, Randhawa GS (1968) Effect of gibberellin on seeded Vitis vinifera with special reference to induction of seedlessness. Vitis 7:10–21Google Scholar
  11. de Jong M, Wolters-Arts M, Feron R, Mariani C, Vriezen WH (2009) The Solanum lycopersicum AUXIN RESPONSE FACTOR 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J 57:160–70CrossRefPubMedGoogle Scholar
  12. Dresselhaus T, Franklin-Tong N (2013) Male-female crosstalk during pollen germination, tube growth and guidance, and double fertilization. Mol Plant 6:1018–1036CrossRefPubMedGoogle Scholar
  13. Dumas C, Gaude T (2006) Fertilization in plants: is calcium a key player? Semin Cell Dev Biol 17:244–253CrossRefPubMedGoogle Scholar
  14. Franklin-Tong VE (1999) Signaling in pollination. Curr Opin Plant Biol 2:490–495CrossRefPubMedGoogle Scholar
  15. Jung CJ, Hur YY, Jung SM, Noh JH, Do GR, Park SJ, Nam JC, Park KS, Hwang HS et al (2014) Transcriptional changes of gibberellin oxidase genes in grapevines with or without gibberellin application during inflorescence development. J Plant Res 127: 359–371CrossRefPubMedGoogle Scholar
  16. Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. CRC Crit Rev Plant Sci 19:479–509CrossRefGoogle Scholar
  17. Koike S, Matsukura C, Takayama M, Asamizu E, Ezura H (2013) Suppression of γ-aminobutyric acid (GABA) transaminases induces prominent GABA accumulation, dwarfism and infertility in the tomato (Solanum lycopersicum L.). Plant Cell Physiol 54:793–807CrossRefPubMedGoogle Scholar
  18. Konrad KR, Wudick MM, Feijó JA (2011) Calcium regulation of tip growth: new genes for old mechanisms. Curr Opin Plant Biol 14:721–730CrossRefPubMedGoogle Scholar
  19. Ling Y, Chen T, Jing Y, Fan L, Wan Y, Lin J (2013) γ-Aminobutyric acid (GABA) homeostasis regulates pollen germination and polarized growth in Picea wilsonii. Planta 238:831–843CrossRefPubMedGoogle Scholar
  20. Lu J, Lamikanra O, Leong S (1997) Induction of seedlessness in ‘Triumph’ muscadine grape (Vitis rotundifolia Michx) by applying gibberellic acid. HortScience 32:89–90Google Scholar
  21. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC et al (2011) CDD: a Conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39:D225–D229CrossRefPubMedGoogle Scholar
  22. Miyashita Y, Good AG (2008) Contribution of the GABA shunt to hypoxia-induced alanine accumulation in roots of Arabidopsis thaliana. Plant Cell Physiol 49:92–102CrossRefPubMedGoogle Scholar
  23. Ohra I, Ariyoshi S (1979) Comparison of protein precipitants for the determination of free amino acids in plasma. Agric Biol Chem 43:1473–1478Google Scholar
  24. Okamoto G, Miura K (2005) Effect of pre-bloom GA application on pollen tube growth in cv. Delaware grape pistils. Vitis 44: 157–159Google Scholar
  25. Ozga JA, Reinecke DM (2003) Hormonal interactions in fruit development. J Plant Growth Regul 22:73–81CrossRefGoogle Scholar
  26. Palanivelu R, Brass L, Edlund AF, Preuss D (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114:47–59CrossRefPubMedGoogle Scholar
  27. Pandolfini T (2009) Seedless Fruit Production by Hormonal Regulation of Fruit Set. Nutrients 1:168–77CrossRefPubMedPubMedCentralGoogle Scholar
  28. Park KS, Yun HK, Suh HS, Jeong SB, Cho HM (2004) Breeding of early season grape cultivar ‘Tamnara’ (Vitis hybrid) with high quality and disease resistance. Korean J Hortic Sci Technol 22:458–461Google Scholar
  29. Park YS, Heo JY, Park SM (2016) Production of hypo-and hypertetraploid seedlings from open-, self-, and cross-pollinated hypo-and hypertetraploid grape. Korean J Hortic Sci Technol 34:771–778Google Scholar
  30. Ramesh SA, Tyerman SD, Xu B, Bose J, Kaur S, Conn V, Domingos P, Ullah S, Wege S et al (2015) GABA signaling modulates plant growth by directly regulating the activity of plant-specific anion transporters. Nat Commun 6:7879CrossRefPubMedPubMedCentralGoogle Scholar
  31. Renault H, Roussel V, El Amrani A, Arzel M, Renault D, Bouchereau A, Deleu C (2010) The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol 10:20CrossRefPubMedPubMedCentralGoogle Scholar
  32. Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4:446–452CrossRefPubMedGoogle Scholar
  33. Takayama M, Koike S, Kusano M, Matsukura C, Saito K, Ariizumi T, Ezura H (2015) Tomato glutamate decarboxylase genes SlGAD2 and SlGAD3 play key roles in regulating γ-aminobutyric acid levels in tomato (Solanum lycopersicum). Plant Cell Physiol 56:1533–45CrossRefPubMedGoogle Scholar
  34. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  35. Vergara R, Parada F, Rubio S, Pérez FJ (2012) Hypoxia induces H2O2 production and activates antioxidant defence system in grapevine buds through mediation of H2O2 and ethylene. J Exp Bot 63:4123–4131CrossRefPubMedPubMedCentralGoogle Scholar
  36. Vergara R, Parada F, Pérez FJ (2013) Is GABA-shunt functional in endodormant grapevine buds under respiratory stress? Plant Growth Regul 71:253–260CrossRefGoogle Scholar
  37. Wittwer SH, Bukovac MJ, Sell HM, Weller LE (1957) Some effects of gibberellin on flowering and fruit setting. Plant Physiol 32:39–41CrossRefPubMedPubMedCentralGoogle Scholar
  38. Youn YS, Park JK, Jang HD, Rhee YW (2011) Sequential hydration with anaerobic and heat treatment increases GABA (gammaaminobutyric acid) content in wheat. Food Chem 129:1631–1635CrossRefGoogle Scholar
  39. Yu GH, Liang JG, He ZK, Sun MX (2006) Quantum dot-mediated detection of γ-aminobutyric acid binding sites on the surface of living pollen protoplasts in tobacco. Chem Biol 13:723–731CrossRefPubMedGoogle Scholar
  40. Yu GH, Zou J, Feng J, Peng XB, Wu JY, Wu YL, Palanivelu R, Sun MX (2014) Exogenous γ-aminobutyric acid (GABA) affects pollen tube growth via modulating putative Ca 2+ -permeable membrane channels and is coupled to negative regulation on glutamate decarboxylase. J Exp Bot 65:3235–3248CrossRefPubMedPubMedCentralGoogle Scholar
  41. Zhao Y, Liu W, Xu YP, Cao JY, Braam J, Cai XZ (2013) Genome-wide identification and functional analyses of calmodulin genes in Solanaceous species. BMC Plant Biol 13:70CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Korean Society for Horticultural Science and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Chan Jin Jung
    • 1
  • Youn Young Hur
    • 1
  • Jin Seok Moon
    • 1
  • Sung-Min Jung
    • 1
  1. 1.Fruit Research Division, National Institute of Horticultural and Herbal ScienceRural Development AdministrationWanjuRepublic of Korea

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