Journal of Plant Growth Regulation

, Volume 37, Issue 1, pp 101–113 | Cite as

Jasmonate Metabolism and Its Relationship with Abscisic Acid During Strawberry Fruit Development and Ripening

  • Adrián Garrido-Bigotes
  • Pablo M. Figueroa
  • Carlos R. Figueroa


The plant hormone jasmonoyl-isoleucine (JA-Ile) is involved in stress response, development, and secondary metabolite production, although its role in fruit development and ripening remains unknown. The aim of this study is to describe variations of endogenous jasmonate (JAs) contents and JA metabolism-related genes in order to associate these to the evolution of abscisic acid (ABA) content during development and ripening of strawberry (Fragaria × ananassa Duch. cv. Aromas) fruit. A quantitative analysis of phytohormones and gene expression was carried out using liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS) and quantitative reverse transcription PCR (RT-qPCR) assays, respectively. The expression of genes encoding for JA metabolism enzymes exhibited a significant decrease concomitant to reduction of JAs and an increment of ABA levels from flowering to ripening stages. Exogenous application of methyl jasmonate (MeJA) triggered anthocyanin accumulation along with an increase in JA-Ile, JA, and MeJA levels, and a concomitant decrease in ABA. Together, these results provide insights into JAs homeostasis during strawberry fruit development, suggesting that MeJA-induced anthocyanin accumulation could be mediated by the activation of the JA signaling pathway. Furthermore, we propose an antagonistic relationship from the JA to the ABA pathway during non-climacteric strawberry fruit development and ripening.


Abscisic acid (ABA) Anthocyanins Fragaria × ananassa Fruit development and ripening Jasmonoyl-isoleucine (JA-Ile) Oxylipins 



A.G.-B. acknowledges the support by the CONICYT [Grant ‘Beca Doctorado Nacional 2015 No. 21151411’]. C.R.F. thanks to the CONICYT for the acquisition of the colorimeter and texture analyzer [Grant PIA/ACT-1110]. The authors are grateful for the help of S.V. Smalley in editing the English language throughout the manuscript. In addition, the Danforth Plant Science Center offers their thanks to the National Science Foundation (NSF, USA) for the acquisition of the QTRAP LC-MS/MS [Grant No. DBI-1427621].


This study was funded by the National Commission for Technological and Scientific Research (CONICYT, Chile) [grant CONICYT, FONDECYT/Regular 1140663 to C.R.F.].

Author Contributions

AG-B conducted experiments, analyzed data, prepared figures and tables, and wrote the manuscript; PMF analyzed data, wrote, and edited the manuscript; and CRF conceived and designed research, obtained research fund, analyzed data, prepared figures and tables, wrote, and edited the manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

344_2017_9710_MOESM1_ESM.docx (2.2 mb)
Supplementary material 1 (DOCX 2264 KB)


  1. Aubert Y, Widemann E, Miesch L et al (2015) CYP94-mediated jasmonoyl-isoleucine hormone oxidation shapes jasmonate profiles and attenuates defence responses to Botrytis cinerea infection. J Exp Bot 66:3879–3892. doi: 10.1093/jxb/erv190 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Böttcher C, Burbidge CA, di Rienzo V et al (2015) Jasmonic acid-isoleucine formation in grapevine (Vitis vinifera L.) by two enzymes with distinct transcription profiles. J Integr Plant Biol 57:618–627. doi: 10.1111/jipb.12321 CrossRefPubMedGoogle Scholar
  3. Carbone F, Preuß A, De Vos RCH et al (2009) Developmental, genetic and environmental factors affect the expression of flavonoid genes, enzymes and metabolites in strawberry fruits. Plant Cell Environ 32:1117–1131. doi: 10.1111/j.1365-3040.2009.01994.x CrossRefPubMedGoogle Scholar
  4. Cherian S, Figueroa CR, Nair H (2014) “Movers and shakers” in the regulation of fruit ripening: a cross-dissection of climacteric versus non-climacteric fruit. J Exp Bot 65:4705–4722. doi: 10.1093/jxb/eru280 CrossRefPubMedGoogle Scholar
  5. Concha CM, Figueroa NE, Poblete LA et al (2013) Methyl jasmonate treatment induces changes in fruit ripening by modifying the expression of several ripening genes in Fragaria chiloensis fruit. Plant Physiol Biochem 70:433–444. doi: 10.1016/j.plaphy.2013.06.008 CrossRefPubMedGoogle Scholar
  6. Flores G, Pérez C, Gil C et al (2013) Methyl jasmonate treatment of strawberry fruits enhances antioxidant activity and the inhibition of nitrite productionin LPS-stimulated Raw 264.7 cells. J Funct Foods 5:1803–1809. doi: 10.1016/j.jff.2013.08.012 CrossRefGoogle Scholar
  7. Gansser D, Latza S, Berger RG (1997) Methyl jasmonates in developing strawberry fruit (Fragaria ananassa Duch. cv. Kent). J Agric Food Chem 45:2477–2480. doi: 10.1021/jf9608940 CrossRefGoogle Scholar
  8. Giné-Bordonaba J, Terry LA (2016) Effect of deficit irrigation and methyl jasmonate application on the composition of strawberry (Fragaria × ananassa) fruit and leaves. Sci Hortic 199:63–70. doi: 10.1016/j.scienta.2015.12.026 CrossRefGoogle Scholar
  9. Goetz S, Hellwege A, Stenzel I et al (2012) Role of cis-12-oxo phytodienoic acid in tomato embryo development. Plant Physiol 158:1715–1727. doi: 10.1104/pp.111.192658 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Jaakola L (2013) New insights into the regulation of anthocyanin biosynthesis in fruits. Trends Plant Sci 18:477–483. doi: 10.1016/j.tplants.2013.06.003 CrossRefPubMedGoogle Scholar
  11. Jia H-F, Chai Y-M, Li C-L et al (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol 157:188–199. doi: 10.1104/pp.111.177311 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Jia H, Wang Y, Sun M et al (2013) Sucrose functions as a signal involved in the regulation of strawberry fruit development and ripening. New Phytol 198:453–465. doi: 10.1111/nph.12176 CrossRefPubMedGoogle Scholar
  13. Jia H, Jiu S, Zhang C et al (2016) Abscisic acid and sucrose regulate tomato and strawberry fruit ripening through the abscisic acid-stress-ripening transcription factor. Plant Biotechnol J 14:2045–2065. doi: 10.1111/pbi.12563 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Jiang Y, Joyce DC (2003) ABA effects on ethylene production, PAL activity, anthocyanin and phenolic contents of strawberry fruit. Plant Growth Regul 39:171–174. doi: 10.1023/A:1022539901044 CrossRefGoogle Scholar
  15. Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229. doi: 10.1016/j.tplants.2015.02.001 CrossRefPubMedGoogle Scholar
  16. Koo YJ, Yoon ES, Seo JS et al (2013) Characterization of a methyl jasmonate specific esterase in Arabidopsis. J Korean Soc Appl Biol Chem 56:27–33. doi: 10.1007/s13765-012-2201-7 CrossRefGoogle Scholar
  17. Lee J, Durst RW, Wrolstad RE (2005) Determination of total monomeric anthocyanin pigment content of fruit juices, beverages, natural colorants, and wines by the pH differential method: collaborative study. J AOAC Int 88:1269–1278PubMedGoogle Scholar
  18. Liao Z, Chen M, Guo L et al (2004) Rapid isolation of high-quality total RNA from taxus and ginkgo. Prep Biochem Biotechnol 34:209–214. doi: 10.1081/PB-200026790 CrossRefPubMedGoogle Scholar
  19. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2[−ΔΔC(T)] method. Methods 25:402–408. doi: 10.1006/meth.2001.1262 CrossRefPubMedGoogle Scholar
  20. Ludwig-Müller J, Jülke S, Bierfreund NM et al (2009) Moss (Physcomitrella patens) GH3 proteins act in auxin homeostasis. New Phytol 181:323–338. doi: 10.1111/j.1469-8137.2008.02677.x CrossRefPubMedGoogle Scholar
  21. McGuire RG (1992) Reporting of objective color measurements. HortScience 27:1254–1255Google Scholar
  22. Meesters C, Mönig T, Oeljeklaus J et al (2014) A chemical inhibitor of jasmonate signaling targets JAR1 in Arabidopsis thaliana. Nat Chem Biol 10:830–836. doi: 10.1038/nchembio.1591 CrossRefPubMedGoogle Scholar
  23. Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc 5:986–992. doi: 10.1038/nprot.2010.37 CrossRefPubMedGoogle Scholar
  24. Preuß A, Augustin C, Figueroa CR et al (2014) Expression of a functional jasmonic acid carboxyl methyltransferase is negatively correlated with strawberry fruit development. J Plant Physiol 171:1315–1324. doi: 10.1016/j.jplph.2014.06.004 CrossRefPubMedGoogle Scholar
  25. Puhl I, Treutter D (2008) Ontogenetic variation of catechin biosynthesis as basis for infection and quiescence of Botrytis cinerea in developing strawberry fruits. J Plant Dis Prot 115:247–251. doi: 10.1007/BF03356272 CrossRefGoogle Scholar
  26. Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343. doi: 10.1146/annurev-phyto-073009-114447 CrossRefPubMedGoogle Scholar
  27. Rosquete MR, Barbez E, Kleine-Vehn J (2012) Cellular auxin homeostasis: gatekeeping is housekeeping. Mol Plant 5:772–786. doi: 10.1093/mp/ssr109 CrossRefPubMedGoogle Scholar
  28. Saavedra GM, Figueroa NE, Poblete LA et al (2016) Effects of preharvest applications of methyl jasmonate and chitosan on postharvest decay, quality and chemical attributes of Fragaria chiloensis fruit. Food Chem 190:448–453. doi: 10.1016/j.foodchem.2015.05.107 CrossRefPubMedGoogle Scholar
  29. Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571. doi: 10.3389/fpls.2016.00571 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Schaller A, Stintzi A (2009) Enzymes in jasmonate biosynthesis—structure, function, regulation. Phytochemistry 70:1532–1538. doi: 10.1016/j.phytochem.2009.07.032 CrossRefPubMedGoogle Scholar
  31. Scholz SS, Reichelt M, Boland W, Mithöfer A (2015) Additional evidence against jasmonate-induced jasmonate induction hypothesis. Plant Sci 239:9–14. doi: 10.1016/j.plantsci.2015.06.024 CrossRefPubMedGoogle Scholar
  32. Seo HS, Song JT, Cheong JJ et al (2001) Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc Natl Acad Sci USA 98:4788–4793. doi: 10.1073/pnas.081557298 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Shan X, Zhang Y, Peng W et al (2009) Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. J Exp Bot 60:3849–3860. doi: 10.1093/jxb/erp223 CrossRefPubMedGoogle Scholar
  34. Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127. doi: 10.1105/tpc.104.023549 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Stintzi A, Weber H, Reymond P et al (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc Natl Acad Sci 98:12837–12842. doi: 10.1073/pnas.211311098 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Suza WP, Staswick PE (2008) The role of JAR1 in jasmonoyl-l-isoleucine production during Arabidopsis wound response. Planta 227:1221–1232. doi: 10.1007/s00425-008-0694-4 CrossRefPubMedGoogle Scholar
  37. Symons GM, Chua Y-J, Ross JJ et al (2012) Hormonal changes during non-climacteric ripening in strawberry. J Exp Bot 63:4741–4750. doi: 10.1093/jxb/ers147 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697. doi: 10.1093/aob/mcm079 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Wasternack C, Kombrink E (2010) Jasmonates: structural requirements for lipid-derived signals active in plant stress responses and development. ACS Chem Biol 5:63–77. doi: 10.1021/cb900269u CrossRefPubMedGoogle Scholar
  40. Widemann E, Smirnova E, Aubert Y et al (2016) Dynamics of jasmonate metabolism upon flowering and across leaf stress responses in Arabidopsis thaliana. Plants 5:4. doi: 10.3390/plants5010004 CrossRefPubMedCentralGoogle Scholar
  41. Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223. doi: 10.1016/S1369-5266(02)00256-X CrossRefPubMedGoogle Scholar
  42. Woldemariam MG, Onkokesung N, Baldwin IT, Galis I (2012) Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulates jasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores. Plant J Cell Mol Biol 72:758–767. doi: 10.1111/j.1365-313X.2012.05117.x CrossRefGoogle Scholar
  43. Yuan Z, Zhang D (2015) Roles of jasmonate signalling in plant inflorescence and flower development. Curr Opin Plant Biol 27:44–51. doi: 10.1016/j.pbi.2015.05.024 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Phytohormone Research Laboratory, Institute of Biological SciencesUniversity of TalcaTalcaChile
  2. 2.Faculty of Forest SciencesUniversity of ConcepciónConcepciónChile

Personalised recommendations