Skip to main content
SpringerLink
Log in

Early Methyl Jasmonate Application to Peach Delays Fruit/Seed Development by Altering the Expression of Multiple Hormone-Related Genes

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Jasmonates (JAs) play a role in the responses to environmental stress and during growth processes, including fruit/seed development. To better understand the molecular basis of the developmental control exerted by JAs in fruit and seed, methyl jasmonate (MJ, 0.80 mM) was applied to peach fruit (Prunus persica var. laevis Gray) at an early (S1) developmental stage and under field conditions. Mesocarp and seed were sampled at time intervals until ripening; at harvest, MJ-treated fruit were less ripe than controls as assessed by a nondestructive device called a DA-meter. Real-time reverse-transcription polymerase chain reaction analyses revealed that JA-related gene expression (AOS1 and JAZs) was affected early (24 h) after treatment, whereas peaks in transcript accumulation of mesocarp (CYCD3, RD22, SP, Aux/IAA) and seed (PRP, SSADH, PRU, LEA) developmental marker genes were shifted in accord with a developmental slowing down. At ripening (S4), in the mesocarp the upregulation of the ethylene biosynthetic genes ACO1 and ACS1 and of the softening-related genes PG and EXP2 was dramatically counteracted by MJ. Ethylene signaling (ETR1, ETR2) was also affected. Because JAs cross-talk with other hormones, the transcript amounts of major hormone-related genes such as GH3, IAA-AH, NCED, and GA2ox were evaluated and showed changes that further support the hypothesis of delay of the developmental program.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bartel B, Fink GR (1995) ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates. Science 268:1745–1748

    Article  CAS  PubMed  Google Scholar 

  • Bonghi C, Trainotti L, Botton A, Tadiello A, Rasori, Ziliotto F, Zaffalon V, Casadoro G, Ramina A (2011) A microarray approach to identify genes involved in seed-pericarp cross-talk and development in peach. BMC Plant Biol 11:107

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Böttcher C, Keyzers RA, Boss PK, Davies C (2010) Sequestration of auxin by the indole-3-acetic acid-amido synthetase GH3-1 in grape berry (Vitis vinifera L.) and the proposed role of auxin conjugation during ripening. J Exp Bot 61:3615–3625

    Article  PubMed  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Report 11:113–116

    Article  CAS  Google Scholar 

  • Cipollini D (2010) Constitutive expression of methyl jasmonate-inducible responses delays reproduction and constrains fitness responses to nutrients in Arabidopsis thaliana. Evol Ecol 24:59–68

    Article  Google Scholar 

  • Costa G, Noferini M, Fiore G (2005) Metodo ed apparato per determinare la qualità di prodotti ortofrutticoli. Italy Patent No. MO2005000211, University of Bologna

  • Dardick C, Callahan AM, Chiozzotto R, Schaffer RJ, Piagnani MC, Scorza R (2010) Stone formation in peach fruit exhibits spatial coordination of the lignin and flavonoid pathways and similarity to Arabidopsis dehiscence. BMC Biol 8:13

    Article  PubMed Central  PubMed  Google Scholar 

  • Devoghalaere F, Doucen T, Guitton B, Keeling J, Payne W, Ling TJ, Ross JJ, Hallett IC, Gunaseelan K, Dayatilake GA, Diak R, Breen KC, Tustin DS, Costes E, Chagné D, Schaffer RJ, David KM (2012) A genomics approach to understanding the role of auxin in apple (Malus x domestica) fruit size control. BMC Plant Biol 12:7

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fan X, Mattheis JP, Fellman JK (1998) A role for jasmonate in climacteric fruit ripening. Planta 204:444–449

    Article  CAS  Google Scholar 

  • Feys BJF, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male-sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751–759

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Finkelstein RR (2004) The role of hormones during seed development and germination. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action!. Kluwer Academic, Dordrecht, pp 513–537

    Google Scholar 

  • Ghiani A, Onelli E, Aina R, Cocucci M, Citterio S (2011) A comparative study of melting and non-melting flesh peach cultivars reveals that during fruit ripening endopolygalacturonase (endo-PG) is mainly involved in pericarp textural changes, not in firmness reduction. J Exp Bot 62:4043–4054

    Article  CAS  PubMed  Google Scholar 

  • Goetz S, Hellwege A, Stenzel I, Kutter C, Hauptmann V, Forner S, McCaig B, Hause G, Miersch O, Wasternack C, Hause B (2012) Role of cis-12-oxo-phytodienoic acid in tomato embryo development. Plant Physiol 158:1715–1727

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Goossens A, Hakkinen ST, Laakso I, Seppanen-Laakso T, Biondi S, De Sutter V, Lammertyn F, Nuutila AM, Soderlund H, Zabeau M, Inze D, Oksman-Caldentey K-M (2003) A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proc Natl Acad Sci USA 100:8595–8600

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Han YY, Li AX, Li F, Zhao MR, Wang W (2012) Characterization of a wheat (Triticum aestivum L.) expansin gene, TaEXPB23, involved in the abiotic stress response and phytohormone regulation. Plant Physiol Biochem 54:49–58

    Article  CAS  PubMed  Google Scholar 

  • Hayama H, Ito A, Moriguchi T, Kashimura Y (2003) Identification of a new expansin gene closely associated with peach fruit softening. Postharvest Biol Technol 2:1–10

    Article  Google Scholar 

  • Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272

    Article  CAS  PubMed  Google Scholar 

  • Howe GA, Lee GI, Itoh A, Li L, De Rocher AE (2000) Cytochrome P450-dependent metabolism of oxylipins in tomato. Cloning and expression of allene oxide synthase and fatty acid hydroperoxide lyase. Plant Physiol 123:711–724

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ismail A, Riemann M, Nick P (2012) The jasmonate pathway mediates salt tolerance in grapevines. J Exp Bot 63:2127–2139

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kanno Y, Jikumaru Y, Hanada A, Nambara E, Abrams SR, Kamiya Y, Seo M (2010) Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant Cell Physiol 51:1988–2001

    Article  CAS  PubMed  Google Scholar 

  • Kaush KD, Sobolev AP, Goyal RK, Fatima T, Laila-Beevi R, Saftner RA, Handa AK, Mattoo AK (2012) Methyl jasmonate deficiency alters cellular metabolome, including the aminome of tomato (Solanum lycopersicum L.) fruit. Amino Acids 42:843–856

    Article  Google Scholar 

  • Kazan K, Manners JM (2011) JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 17:22–31

    Article  PubMed  Google Scholar 

  • Kondo S, Tomyiama A, Seto H (2000) Changes of endogenous jasmonic acid and methyl jasmonate in apples and sweet cherries during fruit development. J Am Soc Hortic Sci 125:282–287

    CAS  Google Scholar 

  • Kondo S, Yamada H, Setha S (2007) Effects of jasmonates differed at fruit ripening stages on 1-aminocyclopropane-1-carboxylate (ACC) synthase and ACC oxidase gene expression in pears. J Am Soc Hortic Sci 132:120–125

    CAS  Google Scholar 

  • Kubigsteltig I, Laudert D, Weiler EW (1999) Structure and regulation of the Arabidopsis thaliana allene oxide synthase gene. Planta 208:463–471

    Article  CAS  PubMed  Google Scholar 

  • Kumar R, Agarwal P, Tyagi AK, Sharma AK (2012) Genome-wide investigation and expression analysis suggest diverse roles of auxin-responsive GH3 genes during development and response to different stimuli in tomato (Solanum lycopersicum). Mol Genet Genomics 287:221–235

    Article  CAS  PubMed  Google Scholar 

  • Linkies A, Leubner-Metzger G (2012) Beyond gibberellins and abscisic acid: how ethylene and jasmonates control seed germination. Plant Cell Rep 31:253–270

    Article  CAS  PubMed  Google Scholar 

  • Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McConn M, Browse J (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell 8:403–416

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Memelink J (2009) Regulation of gene expression by jasmonate hormones. Phytochemistry 70:1560–1570

    Article  CAS  PubMed  Google Scholar 

  • Muller PY, Janovjak H, Miserez AR, Dobbie Z (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 32:1372–1379

    CAS  PubMed  Google Scholar 

  • Nilo RR, Campos-Vargas R, Orellana A (2012) Assessment of Prunus persica fruit softening using a proteomic approach. J Proteomics 75:1618–1638

    Article  Google Scholar 

  • Ognjanov V, Vujanic-Varga D, Misic PD, Veresbaranji I, Macet K, Tesovic Z, Krstic M, Petrovic N (1995) Anatomical and biochemical studies of fruit development in peach. Sci Hortic 64:33–48

    Article  Google Scholar 

  • Oh Y, Baldwin IT, Gális I (2012) NaJAZh regulates a subset of defense responses against herbivores and spontaneous leaf necrosis in Nicotiana attenuata plants. Plant Physiol 159:769–788

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Overmyer K, Brosché M, Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342

    Article  CAS  PubMed  Google Scholar 

  • Pauwels L, Inzé D, Goossens A (2009) Jasmonate-inducible gene: what does it mean? Trends Plant Sci 14:87–91

    Article  CAS  PubMed  Google Scholar 

  • Payasi A, Sanwal GG (2010) Ripening of climacteric fruits and their control. J Food Biochem 34:679–710

    Article  CAS  Google Scholar 

  • Rohwer CL, Erwin GE (2008) Horticultural application of jasmonates. J Hortic Sci Biotechnol 83:283–304

    CAS  Google Scholar 

  • Soto A, Ruiz KB, Ziosi V, Costa G, Torrigiani P (2012) Ethylene and auxin metabolism and signaling are impaired by methyl jasmonate leading to a transient slowing down of ripening in peach fruit. J Plant Physiol 169:1858–1865

    Article  CAS  PubMed  Google Scholar 

  • Srivastava A, Handa AK (2005) Hormonal regulation of tomato fruit development: a molecular perspective. J Plant Growth Regul 24:67–82

    Article  CAS  Google Scholar 

  • Staswick P, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SH, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–665

    Article  CAS  PubMed  Google Scholar 

  • Tonutti P, Bonghi C, Ruperti B, Tornielli GB, Ramina A (1997) Ethylene evolution and 1-aminocyclopropane-1-carboxylate oxidase gene expression during early development and ripening of peach fruit. J Am Soc Hortic Sci 122:642–647

    CAS  Google Scholar 

  • Torrigiani P, Fregola F, Ziosi V, Ruiz KB, Kondo S, Costa G (2012a) Differential expression of allene oxide synthase (AOS), and jasmonate relationship with ethylene biosynthesis in seed and mesocarp of developing peach fruit. Postharvest Biol Technol 63:67–73

    Article  CAS  Google Scholar 

  • Torrigiani P, Bressanin D, Ruiz Carrasco K, Tadiello A, Trainotti L, Bonghi C, Ziosi V, Costa G (2012b) Spermidine application to young developing peach fruits leads to a slowing down of ripening by impairing ripening-related ethylene and auxin metabolism and signaling. Physiol Plant 146:86–98

    Article  CAS  PubMed  Google Scholar 

  • Trainotti L, Zanin D, Casadoro G (2003) A cell wall-oriented genomic approach reveals a new and unexpected complexity of the softening in peaches. J Exp Bot 54:1821–1832

    Article  CAS  PubMed  Google Scholar 

  • Trainotti L, Bonghi C, Ziliotto F, Zanin D, Rasori A, Casadoro G, Ramina R, Tonutti P (2006) The use of microarray μPeach1.0 to investigate transcriptome changes during transition from pre-climacteric to climacteric phase in peach fruit. Plant Sci 170:606–614

    Article  CAS  Google Scholar 

  • Trainotti L, Tadiello A, Casadoro G (2007) The involvement of auxin in the ripening of climacteric fruits comes of age: the hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches. J Exp Bot 58:3299–3308

    Article  CAS  PubMed  Google Scholar 

  • Wasternack C (2007) Jasmonates, an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wasternack C, Forner S, Strnad M, Hause B (2013) Jasmonates in flower and seed development. Biochimie 95:79–85

    Article  CAS  PubMed  Google Scholar 

  • Yang DL, Yao J, Mei CS, Tong XH, Zeng LH, Li Q, Xiao LT, Sun TP, Li J, Deng XW, Lee CM, Thomashow MF, Yang YN, He ZH, Yang, He SY (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci USA 109:E1192–E1200

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yu M, Shen L, Fan B, Zhao D, Zhen Y, Sheng J (2009) The effect of MeJA on ethylene biosynthesis and induced disease resistance to Botrytis cinerea in tomato. Postharvest Biol Technol 54:153–158

    Article  CAS  Google Scholar 

  • Zanchin A, Bonghi C, Casadoro G, Ramina A, Rascio N (1994) Cell enlargement and cell separation during peach fruit development. Int J Plant Sci 155:49–56

    Article  Google Scholar 

  • Zhang M, Ping L, Zhang G, Li X (2009) Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) genes encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits. J Plant Physiol 166:1241–1252

    Article  CAS  PubMed  Google Scholar 

  • Zhu Z, An F, Feng Y, Li P, Xue L, M A, Jiang Z, Kim JM, To TK, Li W, Zhang X, Yu Q, Dong Z, Chen WQ, Seki M, Zhou JM, Guo H (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci USA 108:12539–12544

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ziegler J, Stenzel I, Hause B, Maucher H, Hamberg M, Grimm R, Ganal M, Wasternack C (2010) Molecular cloning of allene oxide cyclase: the enzyme establishing the stereochemistry of octadecanoids and jasmonates. J Biol Chem 594:19132–19138

    Google Scholar 

  • Ziliotto F, Begheldo M, Rasori A, Bonghi C, Tonutti P (2008) Transcriptome profiling of ripening nectarine (Prunus persica L. Batsch) fruit treated with 1-MCP. J Exp Bot 59:2781–2791

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ziosi V, Bonghi C, Bregoli AM, Trainotti L, Biondi S, Setha S, Kondo S, Costa G, Torrigiani P (2008a) Jasmonate-induced transcriptional changes suggest a negative interference with the ripening syndrome in peach fruit. J Exp Bot 59:563–573

    Article  CAS  PubMed  Google Scholar 

  • Ziosi V, Noferini M, Fiori G, Tadiello A, Trainotti L, Casadoro G, Costa G (2008b) A new index based on Vis spectroscopy to characterize the progression of ripening in peach fruit. Postharvest Biol Technol 49:319–329

    Article  CAS  Google Scholar 

  • Ziosi V, Bregoli AM, Fregola F, Costa G, Torrigiani P (2009) Jasmonate-induced ripening delay is associated with up-regulation of polyamine levels in peach fruit. J Plant Physiol 166:938–946

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by funds PRIN 2007 (project 20074AX5CA_003: Seed and fruit development in peach, phenol and jasmonate metabolism, expressed genes and related markers) from the Italian MIUR to PT. The authors thank Daniela Bressanin for collaboration and Stefania Biondi for critical reading of the manuscript and helpful criticism.

Author information

Authors and Affiliations

  1. Department of Agricultural Sciences (DipSA), University of Bologna, Viale Fanin 46, 40127, Bologna, Italy

    Karina Beatriz Ruiz, Vanina Ziosi, Guglielmo Costa & Patrizia Torrigiani

  2. Department of Biology, University of Padova, Viale G. Colombo 3, 35121, Padova, Italy

    Livio Trainotti

  3. Department of Environmental Agronomy and Crop Science, University of Padova, 35020, Legnaro, Padova, Italy

    Claudio Bonghi

Authors
  1. Karina Beatriz Ruiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Livio Trainotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claudio Bonghi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vanina Ziosi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guglielmo Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Patrizia Torrigiani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patrizia Torrigiani.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 46 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ruiz, K.B., Trainotti, L., Bonghi, C. et al. Early Methyl Jasmonate Application to Peach Delays Fruit/Seed Development by Altering the Expression of Multiple Hormone-Related Genes. J Plant Growth Regul 32, 852–864 (2013). https://doi.org/10.1007/s00344-013-9351-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-013-9351-7

Keywords

Search

Navigation