Gibberellic Acid Induces Unique Molecular Responses in ‘Thompson Seedless’ Grapes as Revealed by Non-targeted Metabolomics

Abstract

Compact clusters and small berry size are the major problems associated with the commercialization of table grapes. The application of gibberellic acid 3 (GA3) has been a long-followed practice to overcome these issues. To analyze the molecular response of ‘Thompson Seedless’ grapes to GA3 treatment, we investigated the metabolomes of its rachises, clusters, and berries, 6 h and 24 h after the treatment. Metabolite profiling using non-targeted metabolomics approach revealed several metabolites, including arginine, proline, tyrosine, kaempferol, resveratrol, catechin, and so on as possible biomarkers of GA3 treatment in grapes. GA3 treatment greatly impacted the alanine, aspartate, and glutamate metabolism pathways, and the GA3-mediated alterations in the levels of certain plant growth regulators and primary metabolites were in accordance with important growth and developmental processes in grapes. This study highlights the effect of GA3 on the profiles of certain polyphenols impacting the flavone and flavonol biosynthesis pathways and hence the nutritional aspect of grapes. The results of this study would be useful to develop self-elongating varieties simplifying the grape cultivation.

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References

  1. Adams DO (2006) Phenolics and ripening in grape berries. Am J Enol Vitic 57:249–256

    CAS  Google Scholar 

  2. Adsule PG, Karibasappa GS, Sawant IS et al (2013) Good agricultural practices for quality table grapes. ICAR-National Research Centre for Grapes, Pune, p 57

    Google Scholar 

  3. Aharoni A, Galili G (2011) Metabolic engineering of the plant primary–secondary metabolism interface. Curr Opin Biotechnol 22:239–244. https://doi.org/10.1016/j.copbio.2010.11.004

    CAS  Article  PubMed  Google Scholar 

  4. Alhadi FA, Jabr M, Yasseen BT (1999) Water stress and gibberellic acid effects on growth of fenugreek plants. Irrig Sci 18:185–190. https://doi.org/10.1007/s002710050061

    Article  Google Scholar 

  5. Ali MB, Howard S, Chen S et al (2011) Berry skin development in Norton grape: distinct patterns of transcriptional regulation and flavonoid biosynthesis. BMC Plant Biol 11:7. https://doi.org/10.1186/1471-2229-11-7

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Alves Filho EG, Silva LMA, Ribeiro PRV et al (2019) 1H NMR and LC-MS-based metabolomic approach for evaluation of the seasonality and viticultural practices in wines from São Francisco River Valley, a Brazilian semi-arid region. Food Chem 289:558–567. https://doi.org/10.1016/j.foodchem.2019.03.103

    CAS  Article  PubMed  Google Scholar 

  7. Arapitsas P, Scholz M, Vrhovsek U et al (2012) A metabolomic approach to the study of wine micro-oxygenation. PLoS ONE 7:e37783. https://doi.org/10.1371/journal.pone.0037783

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Ashraf M, Karim F, Rasul E (2002) Interactive effects of gibberellic acid (GA3) and salt stress on growth, ion accumulation and photosynthetic capacity of two spring wheat (Triticum aestivum L.) cultivars differing in salt tolerance. Plant Growth Regul 36:49–59. https://doi.org/10.1023/A:1014780630479

    CAS  Article  Google Scholar 

  9. Bollina V, Kumaraswamy GK, Kushalappa AC et al (2010) Mass spectrometry-based metabolomics application to identify quantitative resistance-related metabolites in barley against Fusarium head blight. Mol Plant Pathol 11:769–782. https://doi.org/10.1111/j.1364-3703.2010.00643.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Casanova L, Casanova R, Moret A, Agustí M (2009) The application of gibberellic acid increases berry size of “Emperatriz” seedless grape. Span J Agric Res 7:919–927. https://doi.org/10.5424/sjar/2009074-1105

    Article  Google Scholar 

  11. Chaudhary J, Deshmukh R, Mir ZA, Bhat JA (2019) Metabolomics: an emerging technology for soybean improvement. In: Khoobchandani M, Saxena A (eds) Biotechnology products in everyday life. Springer, Cham, pp 175–186

    Google Scholar 

  12. Coombe BG, McCarthy MG (2000) Dynamics of grape berry growth and physiology of ripening. Aust J Grape Wine Res 6:131–135. https://doi.org/10.1111/j.1755-0238.2000.tb00171.x

    Article  Google Scholar 

  13. da Silva PS, Kirinus MBM, Barreto CF et al (2019) Gibberellic acid reduces clusters rot of ‘Sauvignon Blanc’ grapes. Rev Bras Frutic 41:e486. https://doi.org/10.1590/0100-29452019486

    Article  Google Scholar 

  14. Dennis K, Liu K, Tran V et al (2019) Phytochelatin characterization in commonly consumed plant foods using mass spectrometry-based metabolomics. Curr Dev Nutr 3:P18-122–19. https://doi.org/10.1093/cdn/nzz039.P18-122-19

    Article  Google Scholar 

  15. Dokoozlian NK, Peacock WL (2001) Gibberellic acid applied at bloom reduces fruit set and improves size of “crimson seedless” table grapes. HortScience 36:706–709. https://doi.org/10.21273/HORTSCI.36.4.706

    CAS  Article  Google Scholar 

  16. Duthie GG, Duthie SJ, Kyle JAM (2000) Plant polyphenols in cancer and heart disease: implications as nutritional antioxidants. Nutr Res Rev 13:79–106. https://doi.org/10.1079/095442200108729016

    CAS  Article  PubMed  Google Scholar 

  17. FAOSTAT (2017) Food and Agricultural Organization of the United Nations. https://www.fao.org/faostat/en/#data/QC/

  18. Ferrara G, Mazzeo A, Netti G et al (2014) Girdling, gibberellic acid, and forchlorfenuron: Effects on yield, quality, and metabolic profile of table grape cv. Italia. Am J Enol Vitic 65:381–387. https://doi.org/10.5344/ajev.2014.13139

    CAS  Article  Google Scholar 

  19. Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58:2339–2358. https://doi.org/10.1093/jxb/erm121

    CAS  Article  PubMed  Google Scholar 

  20. Gallie DR (2013) l-Ascorbic acid: a multifunctional molecule supporting plant growth and development. Scientifica (Cairo) 2013:1–24. https://doi.org/10.1155/2013/795964

    CAS  Article  Google Scholar 

  21. Ghelis T, Bolbach G, Clodic G et al (2008) Protein tyrosine kinases and protein tyrosine phosphatases are involved in abscisic acid-dependent processes in Arabidopsis seeds and suspension cells. Plant Physiol 148:1668–1680. https://doi.org/10.1104/pp.108.124594

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Gong B, Sun S, Yan Y et al (2018) Glutathione metabolism and its function in higher plants adapting to stress. Antioxidants and antioxidant enzymes in higher plants. Springer International Publishing, Cham, pp 181–205

    Google Scholar 

  23. Gujjar RS, Karkute SG, Rai A et al (2018) Proline-rich proteins may regulate free cellular proline levels during drought stress in tomato. Curr Sci 114:915. https://doi.org/10.18520/cs/v114/i04/915-920

    CAS  Article  Google Scholar 

  24. Hayat S, Ali B, Ahmad A (2007) Salicylic acid: biosynthesis, metabolism and physiological role in plants. Salicylic acid: a plant hormone. Springer, Dordrecht, pp 1–14

    Google Scholar 

  25. Hildebrandt TM, Nunes Nesi A, Araújo WL, Braun HP (2015) Amino acid catabolism in plants. Mol Plant 8:1563–1579. https://doi.org/10.1016/j.molp.2015.09.005

    CAS  Article  PubMed  Google Scholar 

  26. Igamberdiev AU, Eprintsev AT (2016) Organic acids: the pools of fixed carbon involved in redox regulation and energy balance in higher plants. Front Plant Sci 7:1042. https://doi.org/10.3389/fpls.2016.01042

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kanner J, Frankel E, Granit R et al (1994) Natural antioxidants in grapes and wines. J Agric Food Chem 42:64–69. https://doi.org/10.1021/jf00037a010

    CAS  Article  Google Scholar 

  28. Kavi Kishor PB (2015) Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Front Plant Sci 6:1–17. https://doi.org/10.3389/fpls.2015.00544

    Article  Google Scholar 

  29. Kende H, van der Knaap E, Cho H (1998) Deepwater rice: a model plant to study stem elongation. Plant Physiol 118:1105–1110. https://doi.org/10.1104/pp.118.4.1105

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Khan MNMA, Gautam C, Mohammad F et al (2006) Effect of gibberellic acid spray on performance of tomato. Turk J Biol 30:11–16

    CAS  Google Scholar 

  31. Kok D, Bal E (2017) Chemical and non-chemical thinning treatments influence berry growth and composition of Cv. shiraz wine grape (V. vinifera L.). Erwerbs-Obstbau 59:269–273. https://doi.org/10.1007/s10341-017-0321-2

    Article  Google Scholar 

  32. Koukourikou M, Zioziou E, Pantazaki A et al (2015) Effects of gibberellic acid and putrescine on “Thompson Seedless” grapes. Am Int J Biol 3:19–29. https://doi.org/10.15640/aijb.v3n2a2

    Article  Google Scholar 

  33. Li S, Zhang Y, Ding C et al (2019) Proline-rich protein gene PdPRP regulates secondary wall formation in poplar. J Plant Physiol 233:58–72. https://doi.org/10.1016/j.jplph.2018.12.007

    CAS  Article  PubMed  Google Scholar 

  34. Mattioli R, Marchese D, D’Angeli S et al (2008) Modulation of intracellular proline levels affects flowering time and inflorescence architecture in Arabidopsis. Plant Mol Biol 66:277–288. https://doi.org/10.1007/s11103-007-9269-1

    CAS  Article  PubMed  Google Scholar 

  35. Ouma G (2008) Use of gibberellins to improve fruit set in pears after frost damage. J Biol Sci 8:213–216. https://doi.org/10.3923/jbs.2008.213.216

    CAS  Article  Google Scholar 

  36. Owen OE, Kalhan SC, Hanson RW (2002) The key role of anaplerosis and cataplerosis for citric acid cycle function. J Biol Chem 277:30409–30412. https://doi.org/10.1074/jbc.R200006200

    CAS  Article  Google Scholar 

  37. Paleg LG (1965) Physiological effects of gibberellins. Annu Rev Plant Physiol 16:291–322. https://doi.org/10.1146/annurev.pp.16.060165.001451

    CAS  Article  Google Scholar 

  38. Patil SS, Prashant R, Kadoo NY et al (2019) Global study of MFS superfamily transporters in Arabidopsis and grapes reveals their functional diversity in plants. Plant Gene. https://doi.org/10.1016/j.plgene.2019.100179

    Article  Google Scholar 

  39. Pérez FJ, Gómez M (2000) Possible role of soluble invertase in the gibberellic acid berry-sizing effect in Sultana grape. Plant Growth Regul 30:111–116. https://doi.org/10.1023/A:1006318306115

    Article  Google Scholar 

  40. Raskin I (1992) Role of salicylic acid in plants. Annu Rev Plant Physiol Plant Mol Biol 43:439–463. https://doi.org/10.1146/annurev.pp.43.060192.002255

    CAS  Article  Google Scholar 

  41. Reynolds A, Robbins N, Lee HS, Kotsaki E (2016) Impacts and interactions of abscisic acid and gibberellic acid on sovereign coronation and skookum seedless table grapes. Am J Enol Vitic 67:327–338. https://doi.org/10.5344/ajev.2016.15108

    CAS  Article  Google Scholar 

  42. Saccenti E, Hoefsloot HCJ, Smilde AK et al (2014) Reflections on univariate and multivariate analysis of metabolomics data. Metabolomics 10:361–374. https://doi.org/10.1007/s11306-013-0598-6

    CAS  Article  Google Scholar 

  43. Schöppner A, Kindl H (1984) Purification and properties of a stilbene synthase from induced cell suspension cultures of peanut. J Biol Chem 259:6806–6811

    Article  Google Scholar 

  44. Smith CA (2017) LC/MS preprocessing and analysis with xcms. https://bioconductor.riken.jp/packages/3.5/bioc/vignettes/xcms/inst/doc/xcmsPreprocess.pdf

  45. Suehiro Y, Mochida K, Tsuma M et al (2019) Effects of gibberellic acid/cytokinin treatments on berry development and maturation in the yellow-green skinned ‘shine muscat’ grape. Hortic J 88:202–213. https://doi.org/10.2503/hortj.UTD-046

    CAS  Article  Google Scholar 

  46. Sun H, Wang B, Wang J et al (2016) Biomarker and pathway analyses of urine metabolomics in dairy cows when corn stover replaces alfalfa hay. J Anim Sci Biotechnol 7:1–9. https://doi.org/10.1186/s40104-016-0107-7

    CAS  Article  Google Scholar 

  47. Takaki H, Ikeda M, Yamada Y, Harada T (1968) Occurrence of glucosamine in higher plants. Soil Sci Plant Nutr 14:56–61. https://doi.org/10.1080/00380768.1968.10432009

    CAS  Article  Google Scholar 

  48. Upadhyay A, Maske S, Jogaiah S et al (2018) GA3 application in grapes (Vitis vinifera L.) modulates different sets of genes at cluster emergence, full bloom, and berry stage as revealed by RNA sequence-based transcriptome analysis. Funct Integr Genomics 18:439–455. https://doi.org/10.1007/s10142-018-0605-0

    CAS  Article  PubMed  Google Scholar 

  49. Usenik V, Kastelec D, Štampar F (2005) Physicochemical changes of sweet cherry fruits related to application of gibberellic acid. Food Chem 90:663–671. https://doi.org/10.1016/j.foodchem.2004.04.027

    CAS  Article  Google Scholar 

  50. Weaver RJ, Pool RM (1971) Chemical thinning of grape clusters (Vitis vinifera L.). VITIS J Grapevine Res 10:201–209

    CAS  Google Scholar 

  51. Weaver RJ, Shindy W, Kliewer WM (1969) Growth regulator induced movement of photosynthetic products into fruits of “Black Corinth” grapes. Plant Physiol 44:183–188

    CAS  Article  Google Scholar 

  52. Weiss D, Ori N (2007) Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol 144:1240–1246. https://doi.org/10.1104/pp.107.100370

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. Williams LE, Ayars JE (2005) Water use of Thompson Seedless grapevines as affected by the application of gibberellic acid (GA3) and trunk girdling – practices to increase berry size. Agric For Meteorol 129:85–94. https://doi.org/10.1016/j.agrformet.2004.11.007

    Article  Google Scholar 

  54. Winter G, Todd CD, Trovato M et al (2015) Physiological implications of arginine metabolism in plants. Front Plant Sci 6:1–14. https://doi.org/10.3389/fpls.2015.00534

    Article  Google Scholar 

  55. Xia J, Wishart DS, Valencia A (2011) MetPA: a web-based metabolomics tool for pathway analysis and visualization. Bioinformatics 27:2342–2344. https://doi.org/10.1093/bioinformatics/btq418

    CAS  Article  Google Scholar 

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Acknowledgements

UJ acknowledges the Junior and Senior Research Fellowships of the Council of Scientific and Industrial Research (CSIR), India. The authors acknowledge Dr. B. Santhakumari (CSIR-National Chemical Laboratory (CSIR-NCL), Pune, India) for providing the high-resolution Orbitrap liquid chromatography-mass spectrometry (LCMS) facility and Dr. Ramya Prashant (CSIR-NCL), Pune, India, for her guidance during the research. Financial support in the form of Department of Biotechnology (DBT) grants (Project Codes: GAP300026 and GAP319026) and National Agricultural Science Fund (NASF), Indian Council of Agricultural Research (ICAR), India grant (Project Code: GAP311926) to CSIR-NCL are gratefully acknowledged.

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Supplementary file1 (TIF 9855 kb)Online Resource 1 Phenotypic effects of GA3 treatment on ‘Thompson Seedless’ grapes bunch characteristics; (A) 10 mg/L GA3 spray at the rachis stage, (B) 25 mg/L GA3 spray at the cluster stage, and (C) dipping in 25 mg/L GA3 solution at the berry stage.

Supplementary file2 (TIF 2196 kb)Online Resource 2 OPLS-DA score plots showing a clear separation between control and GA3 treated groups at rachis, cluster, and berry stage samples analyzed using the ESI+ mode. Control versus GA3 treated rachises collected at (A) 6 h time-point, (B) 24 h time-point. Control versus GA3 treated clusters collected at (C) 6 h time-point, (D) 24 h time-point. Control versus GA3 treated berries collected at (E) 6 h time-point and (F) 24 h time-point

Supplementary file3 (TIF 2044 kb)Online Resource 3 OPLS-DA score plots showing a clear separation between control and GA3 treated groups at rachis, cluster and berry stage samples analyzed using the ESI mode. Control versus GA3 treated rachises collected at (A) 6 h time-point, (B) 24 h time-point. Control versus GA3 treated clusters collected at (C) 6 h time-point, (D) 24 h time-point. Control versus GA3 treated berries collected at (E) 6 h time-point and (F) 24 h time-point

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Jadhav, U., Mundhe, S., Kumar, Y. et al. Gibberellic Acid Induces Unique Molecular Responses in ‘Thompson Seedless’ Grapes as Revealed by Non-targeted Metabolomics. J Plant Growth Regul 40, 293–304 (2021). https://doi.org/10.1007/s00344-020-10102-7

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Keywords

  • Sultana grapes
  • Untargeted metabolomics
  • GA3 response
  • GA3 signaling
  • Biosynthetic pathways