Skip to main content
SpringerLink
Log in

Methyl jasmonate deficiency alters cellular metabolome, including the aminome of tomato (Solanum lycopersicum L.) fruit

  • Original Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

Exogenous treatment with jasmonates (JA) has been shown to reduce the levels of polyamines in many plants. But the role of endogenous JA on polyamine biosynthesis or other cellular metabolites has thus far remained uninvestigated. We developed transgenic tomato (Solanum lycopersicum L.) having severely reduced methyl JA levels by silencing a fruit ripening-associated lipoxygenase (LOX), SlLoxB, using a truncated LOX gene under the control of the constitutive CaMV35S promoter. The LOX suppressed and MeJA-deficient fruits had lowered polyamine levels. Thus, these transgenic fruits were used as a plant model to evaluate the effects of reduced endogenous MeJA on cellular metabolites in ripening tomato fruits using NMR spectroscopy. During on-shelf ripening, transgenic fruits were significantly reduced in the content of 19 out of 30 metabolites examined, including Ile, Val, Ala, Thr, Asn Tyr, Glu, Gln, His, Phe, Trp, GABA, citrate, succinate, myo-inositol, unidentified compound B, nucleic acid compound Nucl1, choline, and trigonelline as compared to the wild-type azygous counterparts. A significant increase in β-glucose levels in transgenic fruits was observed at the pink stage. The transgenic fruits were equivalent to the wild type in lycopene level and chlorophyll degradation rates. Taken together, these results show that intracellular MeJA significantly regulates overall primary metabolism, especially aminome (amino acids and polyamines) of ripening fruits.

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

Abbreviations

JA:

Jasmonates

MeJA:

Methyl jasmonate

SAM:

S-adenosylmethionine

dab:

Days after breaker

References

  • Baxter CJ, Carrari F, Bauke A, Overy S, Hill SA, Quick PW, Fernie AR, Sweetlove LJ (2005) Fruit carbohydrate metabolism in an introgression line of tomato with increased fruit soluble solids. Plant Cell Physiol 46:425–437

    Article  PubMed  CAS  Google Scholar 

  • Bell E, Creelman RA, Mullet JE (1995) A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc Natl Acad Sci USA 92:8675–8679

    Article  PubMed  CAS  Google Scholar 

  • Bellisle F (1999) Glutamate and the UMAMI taste: sensory, metabolic, nutritional and behavioural considerations. A review of the literature published in the last 10 years. Neurosci Biobehav Rev 23:423–438

    Article  PubMed  CAS  Google Scholar 

  • Biggs MS, Handa AK (1989) Temporal regulation of polygalacturonase gene expression in fruits from normal mutant and heterozygous tomato genotypes. Plant Physiol 89:117–125

    Article  PubMed  CAS  Google Scholar 

  • Biggs MS, Woodson WR, Handa AK (1988) Biochemical basis of high temperature inhibition of ethylene biosynthesis in ripening tomato fruits. Physiol Plant 72:572–578

    Article  CAS  Google Scholar 

  • Biondi S, Scaramagli S, Capitani F, Altamura MM, Torrigiani P (2001) Methyl jasmonate upregulates biosynthetic gene expression, oxidation and conjugation of polyamines, and inhibits shoot formation in tobacco thin layers. J Exp Bot 52:231–242

    Google Scholar 

  • Biondi S, Scoccianti V, Scaramagli S, Ziosi V, Torrigiani P (2003) Auxin and cytokinin modify methyl jasmonate effects on polyamine metabolism and ethylene biosynthesis in tobacco leaf discs. Plant Sci 165:95–101

    Article  CAS  Google Scholar 

  • Bortolotti S, Boggio SB, Delgado L, Orellano EG, Valle EM (2003) Different induction patterns of glutamate metabolising enzymes in ripening fruits of the tomato mutant green flesh. Physiol Plant 119:384–391

    Article  CAS  Google Scholar 

  • Braun S, Kalinowski HO, Berger S (1998) 150 and more basic NMR experiments, 2nd edn. Wiley, Weinheim

    Google Scholar 

  • Burroughs LF (1970) Amino acids. In: Hulme AC (ed) The biochemistry of fruits and their products, vol 1. Academic Press, London, pp 119–146

  • Caroline C, von Dahl, Baldwin IT (2007) Deciphering the role of ethylene in plant—herbivore interactions. J Plant Growth Regul 26:201–209

  • Carrari F, Baxter C, Usadel B, Urbanczyk-Wochniak E, Zanor MI, Nunes-Nesi A, Nikiforova V, Centero D, Ratzka A, Pauly M, Sweetlove LJ, Fernie AR (2006) Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiol 142:1380–1396

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Jones AD, Howe GA (2006) Constitutive activation of the jasmonate signaling pathway enhances the production of secondary metabolites in tomato. FEBS Lett 580:2540–2546

    Article  PubMed  CAS  Google Scholar 

  • Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381

    Article  PubMed  CAS  Google Scholar 

  • Fan TWM (1996) Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog Nucl Magn Reson Spectrosc 28:161–219

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fincato P, Moschou PN, Spedaletti V, Tavazza R, Angelini R, Federico R, Roubelakis-Angelakis KA, Tavladoraki P (2010) Functional diversity inside the Arabidopsis polyamine oxidase gene family. J Exp Bot 62:1155–1168

    Article  PubMed  Google Scholar 

  • Gallardo F, Canton FR, Garcia-Gutierrez A, Canovas FM (1993) Changes in photorespiratory enzymes and glutamate synthases in ripening tomatoes. Plant Physiol Biochem 31:189–196

    CAS  Google Scholar 

  • Goldsbrough PH, Cullis CA (1981) Characterization of the genes for ribosomal RNA in flax. Nucl Acids Res 9:1301–1309

    Article  PubMed  CAS  Google Scholar 

  • Grierson D, Slater A, Maunders M, Crookes P, Tucker GA, Schuch W, Edwards K (1985) Control of ethylene synthesis and ripening by sense and antisense genes in transgenic plants. In: Roberts JA, Tucker GA (eds) Ethylene and plant development. Butterworth, London, pp 147–161

  • Haggag WM, Abd-El-Kareem F (2009) Methyl jasmonate stimulates polyamines biosynthesis and resistance against leaf rust in wheat plants. Arch Phytopath Plant Protec 42:16-31

    Google Scholar 

  • Handa AK, Kausch KD (2002) Improvement of fruit quality by inhibiting production of lipoxygenase in fruits. United States Patent Number 6355862, Issued on March 12, 2002

  • Handa AK, Mattoo AK (2010) Differential and functional interactions emphasize the multiple roles of polyamines in plants. Plant Physiol Biochem 48:540–546

    Article  PubMed  CAS  Google Scholar 

  • Handa AK, Singh NK, Biggs MS (1985) Effect of tunicamycin on in vitro ripening of tomato pericarp tissue. Physiol Plant 63:417–424

    Article  CAS  Google Scholar 

  • Hanik N, Gomez S, Best M, Schueller M, Orians CM, Ferrieri RA (2010) Partitioning of new carbon as 11C in Nicotiana tabacum reveals insight into methyl jasmonate induced changes in metabolism. J Chem Ecol 36:1058–1067

    Article  PubMed  CAS  Google Scholar 

  • Imanishi S, Nagata M (2003) The effect of methyl jasmonate on expression of the genes involved in ethylene biosynthesis in tomato fruits. Abst. 169. American Society of Plant Biologists, Plant Biology 2003, Honolulu

  • Jung C, Lyou S, Yeu S, Kim M, Rhee S, Kim M, Lee J, Choi Y, Cheong J–J (2007) Microarray-based screening of JA-responsive genes in Arabidopsis thaliana. Plant Cell Rep 26:1053–1063

    Article  PubMed  CAS  Google Scholar 

  • Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M (2008) A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol 49:1272–1282

    Article  PubMed  CAS  Google Scholar 

  • Kausch KD, Handa AK (1995) Molecular cloning and nucleotide sequence of a lipoxygenase cDNA from ripening tomato fruit. Plant Physiol 107:669–670

    Article  PubMed  CAS  Google Scholar 

  • Kausch KD, Handa AK (1997) Molecular cloning of a ripening specific lipoxygenase and its expression during wild-type and mutant tomato fruit development. Plant Physiol 113:1041–1050

    Article  PubMed  CAS  Google Scholar 

  • Kevany BM, Tieman DM, Taylor MG, Cin VD, Klee HJ (2007) Ethylene receptor degradation controls the timing of ripening in tomato fruit. Plant J 51:458–467

    Article  PubMed  CAS  Google Scholar 

  • Kondo S, Setha S, Rudell DR, Buchanan DA, Mattheis JP (2005) Aroma volatile biosynthesis in apple affected by 1-MCP and methyljasmonate. Postharvest Biol Technol 36:61–68

    Article  CAS  Google Scholar 

  • Less H, Angelovici R, Tzin V, Galili G (2010) Principal transcriptional regulation and genome-wide system interactions of the Asp-family and aromatic amino acid networks of amino acid metabolism in plants. Amino Acids 39:1023–1028

    Article  PubMed  CAS  Google Scholar 

  • Martens H, Martens M (2001) Multivariate analysis of quality. Wiley, Chichester

    Google Scholar 

  • Martin MN, Cohen JD, Saftner RA (1995) A new 1-aminocyclopropane-1-carboxylic acid-conjugating activity in tomato fruit. Plant Physiol 109:917–926

    Article  PubMed  CAS  Google Scholar 

  • Mattoo AK, Handa AK (2008) Higher polyamines restore and enhance metabolic memory in ripening fruit. Plant Sci 174:386–393

    Article  CAS  Google Scholar 

  • Mattoo AK, Murata T, Pantastico EB, Chachin K, Ogata K, Phan CT (1975) Chemical changes during ripening and senescence. In: Pantastico EB (ed) Postharvest physiology, handling and utilization of tropical and subtropical fruits and vegetables. The AVI Publishing Co, USA, pp 104–127

  • Mattoo AK, Sobolev AP, Neelam A, Goyal RK, Handa AK, Segre AL (2006) Nuclear magnetic resonance spectroscopy-based metabolite profiling of transgenic tomato fruit engineered to accumulate spermidine and spermine reveals enhanced anabolic and nitrogen-carbon interactions. Plant Physiol 142:1759–1770

    Article  PubMed  CAS  Google Scholar 

  • Mattoo AK, Minocha SC, Minocha R, Handa AK (2010) Polyamines and cellular metabolism in plants: transgenic approaches reveal different responses to diamine putrescine versus higher polyamines spermidine and spermine. Amino Acids 38:405–413

    Article  PubMed  CAS  Google Scholar 

  • Mehta RA, Fawcett TW, Porath D, Mattoo AK (1992) Oxidative stress causes rapid membrane translocation and in vivo degradation of ribulose-1, 5-bisphosphate carboxylase/oxygenase. J Biol Chem 267:2810–2816

    PubMed  CAS  Google Scholar 

  • Mehta RA, Warmbardt RD, Mattoo AK (1996) Tomato fruit carboxypeptidase: properties, induction upon wounding, and immunocytochemical localization. Plant Physiol 110:883–892

    PubMed  CAS  Google Scholar 

  • Mehta RA, Cassol T, Li N, Ali N, Handa AK, Mattoo AK (2002) Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality and vine life. Nature Biotech 20:613–618

    Article  CAS  Google Scholar 

  • Mounet F, Lemaire-Chamley M, Maucourt M, Cabasson C, Giraudel J-L, Deborde C, Lessire R, Gallusci P, Bertrand A, Gaudille`re M, Rothan C, Rolin D, Moing A (2007) Quantitative metabolic profiles of tomato flesh and seeds during fruit development: complementary analysis with ANN and PCA. Metabolomics 3:273–288

    Article  CAS  Google Scholar 

  • Nambeesan S, Handa AK, Mattoo AK (2008) Polyamines and regulation of ripening and senescence. In: Paliyath G, Murr DP, Handa AK, Lurie S (eds) Postharvest biology and technology of fruits, vegetables and flowers. Blackwell, Oxford, pp 319–340

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

    Article  PubMed  CAS  Google Scholar 

  • Pawliszyn J (1997) Solid phase microextraction: theory and practice. Wiley, New York

    Google Scholar 

  • Pegg AE (2009) Mammalian polyamine metabolism and function. IUBMB Life 61:880–894

    Article  PubMed  CAS  Google Scholar 

  • Peremarti A, Bassie L, Yuan D, Pelacho A, Christou P, Capell T (2010) Transcriptional regulation of the rice arginine decarboxylase (ADC1) and S-adenosylmethionine decarboxylase (Samdc) genes by methyl jas monate. Plant Physiol Biochem 48:553–559

    Article  PubMed  CAS  Google Scholar 

  • Perez-Amador MA, Leon J, Green PJ, Carbonell J (2002) Induction of the arginine decarboxylase ADC2 gene provides evidence for the involvement of polyamines in the wound response in Arabidopsis. Plant Physiol 130:1454–1463

    Article  PubMed  CAS  Google Scholar 

  • Pratta G, Zorzoli R, Boggio SB, Picardi LA, Valle EM (2004) Glutamine and glutamate levels and related metabolizing enzymes in tomato fruits with different shelf-life. Sci Hortic 100:341–347

    Article  CAS  Google Scholar 

  • Schardl CL, Byrd AD, Benzion G, Altschuler MA, Hildebrand DF, Hunt AG (1987) Design and construction of a versatile system for the expression of foreign genes in plants. Gene 61:1–11

    Article  PubMed  CAS  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–590

    Article  PubMed  CAS  Google Scholar 

  • Sobolev AP, Segre AL, Lamanna R (2003) Proton high-field NMR study of tomato juice. Magn Reson Chem 41:237–245

    Article  CAS  Google Scholar 

  • Sorrequieta A, Ferraro G, Boggio SB, Valle EM (2010) Free amino acid production during tomato fruit ripening: a focus on l-glutamate. Amino Acids 38:1523–1532

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Srivastava A, Chung SH, Fatima T, Datsenka T, Handa AK, Mattoo AK (2007) Polyamines as anabolic growth regulators revealed by transcriptome analysis and metabolite profiles of tomato fruits engineered to accumulate spermidine and spermine. Plant Biotechnol 24:57–70

    Article  CAS  Google Scholar 

  • Tadeo JL, Ortiz JM, Martin B, Estellés A (1988) Changes in the nitrogen content and amino acid composition of navel oranges during ripening. J Sci Food Agric 43:201–209

    Article  CAS  Google Scholar 

  • Tieman DM, Harriman RW, Ramamohan G, Handa AK (1992) An antisense pectin methylesterase gene alters pectin chemistry and soluble solids in tomato fruit. Plant Cell 4:667–679

    Article  PubMed  CAS  Google Scholar 

  • Tzin V, Galili G (2010) New insights into the shikimate and aromatic amino acids biosynthesis pathways in plants. Mol Plant 3:956–972

    Article  PubMed  CAS  Google Scholar 

  • Valle EM, Boggio SB, Heldt HW (1998) Free amino acids content of phloem sap and fruits in Lycopersicon esculentum. Plant Cell Physiol 39:458–461

    CAS  Google Scholar 

  • Van Haute E, Joos H, Maes M, Warren G, van Montagu M, Schell J (1983) Intergenic transfer and exchange recombination of restriction fragments cloned in pBR322: a novel strategy for the reversed genetics of the Ti plasmids of Agrobacterium tumefaciens. EMBO 2:411–417

    Google Scholar 

  • Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Close TJ (2007) Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress. Plant Cel Environ 30:410–421

    Article  CAS  Google Scholar 

  • Walters D, Cowley T, Mitchel A (2002) Methyl jasmonate alters polyamine metabolism and induces systemic protection against powdery mildew infection in barley seedlings. J Exp Bot 53:747–756

    Article  PubMed  CAS  Google Scholar 

  • Yan X, Chen S (2007) Regulation of plant glucosinolate metabolism. Planta 226:1343–1352

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  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  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

Author information

Author notes

  1. Kurt D. Kausch

    Present address: Department of Professional Development, Advocate Illinois Masonic Medical Center, Chicago, IL, 60657-5147, USA

  2. Ravinder K. Goyal

    Present address: Agriculture and Agri-Food Canada-Lethbridge Research Centre, P.O. 3000, 5403-1st Ave South, Lethbridge, AB, T1J 4B1, Canada

  3. Tahira Fatima

    Present address: Department of Biology, The University of Western Ontario, London, ON, Canada

  4. Rekha Laila-Beevi

    Present address: Institute of Landscape Matter Dynamics, Leibniz-Centre for Agricultural Landscape Research (ZALF), Eberswalder Strasse 84, 15374, Muencheberg, Germany

Authors and Affiliations

  1. Department of Horticulture and Landscape Architecture, Purdue University, 625 Agriculture Mall Drive, West Lafayette, IN, 47907-1165, USA

    Kurt D. Kausch & Avtar K. Handa

  2. Istituto di Metodologie Chimiche, Laboratorio di Risonanza Magnetica “Annalaura Segre”, CNR 00015 Monterotondo, Rome, Italy

    Anatoly P. Sobolev & Rekha Laila-Beevi

  3. Sustainable Agricultural Systems Laboratory, The Henry A. Wallace Beltsville Agricultural Research Center, U.S. Department of Agriculture, Agriculture Research Service, Beltsville, MD, 20705-2350, USA

    Ravinder K. Goyal, Tahira Fatima, Robert A. Saftner & Autar K. Mattoo

Authors
  1. Kurt D. Kausch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anatoly P. Sobolev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ravinder K. Goyal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tahira Fatima
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rekha Laila-Beevi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Robert A. Saftner
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Avtar K. Handa
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Autar K. Mattoo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Autar K. Mattoo.

Additional information

Kurt D. Kausch and Anatoly P. Sobolev contributed equally to this paper.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 47 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kausch, K.D., Sobolev, A.P., Goyal, R.K. et al. Methyl jasmonate deficiency alters cellular metabolome, including the aminome of tomato (Solanum lycopersicum L.) fruit. Amino Acids 42, 843–856 (2012). https://doi.org/10.1007/s00726-011-1000-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-011-1000-5

Keywords

Search

Navigation