Skip to main content
Log in

A tomato enzyme synthesizes (+)-7-iso-jasmonoyl-l-isoleucine in wounded leaves

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Jasmonoyl-l-isoleucine (JA-Ile) is a key jasmonate signal that probably functions in all plant species. The JASMONATE RESISTANT 1 (JAR1) enzyme synthesizes JA-Ile in Arabidopsis [Arabidopsis thaliana (L.) Heynh.], but a similar enzyme from tomato [Solanum lycopersicum (L.)] was not previously described. Tomato SlJAR1 has 66% sequence identity with Arabidopsis JAR1 and the SlJAR1-GST fusion protein purified from Escherichia coli catalyzed the formation of JA-amino acid conjugates in vitro. Kinetic analysis showed the enzyme has a strong preference for Ile over Leu and Val and it was about 10-fold more active with (+)-7-iso-JA than with its epimer (−)-JA. Leaf wounding rapidly increased JA-Ile 50-fold to about 450 pmol g−1 FW at 30 min after wounding, while conjugates with Leu, Phe, Val and Met were only marginally increased or not detected. Nearly all of the endogenous JA-Ile was the bioactive epimer (+)-7-iso-JA-Ile and there was no evidence for its conversion to (−)-JA-Ile up to 6 h after wounding. A transgenic RNAi approach was used to suppress SlJAR1 transcript that reduced JA-Ile accumulation by 50–75%, suggesting that other JA conjugating enzymes may be present. These results show that SlJAR1 synthesizes the bioactive conjugate (+)-7-iso-JA-Ile and this is the predominant isomer accumulated in wounded tomato leaves.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

GC/MS:

Gas chromatography/mass spectrometry

GST:

Glutathione S transferase

JA:

Jasmonic acid

JAR:

Jasmonate resistant

JAZ:

Jasmonate ZIM domain

MeJA:

Methyljasmonate

OPDA:

12-Oxo-phytodienoic acid

PCR:

Polymerase chain reaction

PFBB:

2,3,4,5,6-Pentafluorobenzyl bromide

TLC:

Thin-layer chromatography

References

  • Bergey DR, Howe GA, Ryan CA (1996) Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc Natl Acad Sci USA 93:12053–12058

    Article  PubMed  CAS  Google Scholar 

  • Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60:183–205

    Article  PubMed  CAS  Google Scholar 

  • Chang KH, Xiang H, Dunaway-Mariano D (1997) Acyl-adenylate motif of the acyl-adenylate/thioester-forming enzyme superfamily: a site-directed mutagenesis study with the Pseudomonas sp. strain CBS3 4-chlorobenzoate:coenzyme A ligase. Biochem 36:15650–15659

    Article  CAS  Google Scholar 

  • Chico JM, Chini A, Fonseca S, Solano R (2008) JAZ repressors set the rhythm in jasmonate signaling. Curr Opin Plant Biol 11:486–494

    Article  PubMed  CAS  Google Scholar 

  • Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671

    Article  PubMed  CAS  Google Scholar 

  • Chung HS, Koo AJ, Gao X, Jayanty S, Thines B, Jones AD, Howe GA (2008) Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol 146:952–964

    Article  PubMed  CAS  Google Scholar 

  • Chung HS, Niu Y, Browse J, Howe GA (2009) Top hits in contemporary JAZ: an update on jasmonate signaling. Phytochemistry 70:1547–1559

    Article  PubMed  CAS  Google Scholar 

  • Constabel CP, Bergey DR, Ryan CA (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc Natl Acad Sci USA 92:407–411

    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 

  • Epstein E, Cohen JD (1981) Microscale preparation of pentafluorbenzyl esters. Electron-capture gas chromatographic detection of indole-3-acetic acid from plants. J Chromatogr 209:413–420

    Article  CAS  Google Scholar 

  • Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716

    Article  PubMed  CAS  Google Scholar 

  • Feys B, 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  CAS  Google Scholar 

  • Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350

    Article  PubMed  CAS  Google Scholar 

  • Glauser G, Dubugnon L, Mousavi SA, Rudaz S, Wolfender JL, Farmer EE (2009) Velocity estimates for signal propagation leading to systemic jasmonic acid accumulation in wounded Arabidopsis. J Biol Chem 284:34506–34513

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  PubMed  CAS  Google Scholar 

  • Graham JS, Pearce G, Merryweather J, Titani K, Ericsson LH, Ryan CA (1985) Wound-induced proteinase inhibitors from tomato leaves. II. The cDNA-deduced primary structure of pre-inhibitor II. J Biol Chem 260:6561–6564

    PubMed  CAS  Google Scholar 

  • Guranowski A, Miersch O, Staswick PE, Suza W, Wasternack C (2007) Substrate specificity and products of side-reactions catalyzed by jasmonate:amino acid synthetase (JAR1). FEBS Lett 581:815–820

    Article  PubMed  CAS  Google Scholar 

  • Hause B, Stenzel I, Miersch O, Maucher H, Kramell R, Ziegler J, Wasternack C (2000) Tissue-specific oxylipin signature of tomato flowers: allene oxide cyclase is highly expressed in distinct flower organs and vascular bundles. Plant J 24:113–126

    Article  PubMed  CAS  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    Article  PubMed  CAS  Google Scholar 

  • Howe GA, Lightner J, Browse J, Ryan CA (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8:2067–2077

    Article  PubMed  CAS  Google Scholar 

  • Hsieh H-L, Okamoto H, Wang M, Ang L-H, Matsui M, Goodman H, Deng XW (2000) FIN219, an auxin-regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development. Genes Dev 14:1958–1970

    PubMed  CAS  Google Scholar 

  • Kang JH, Wang L, Giri A, Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta. Plant Cell 18:3303–3320

    Article  PubMed  CAS  Google Scholar 

  • Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105:7100–7105

    Article  PubMed  CAS  Google Scholar 

  • Koo AJ, Gao X, Daniel Jones A, Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J 59:974–986

    Article  PubMed  CAS  Google Scholar 

  • Lee GI, Howe GA (2003) The tomato mutant spr1 is defective in system in perception and the production of a systemic wound signal for defense gene expression. Plant J 33:567–576

    Article  PubMed  CAS  Google Scholar 

  • Li L, Li C, Howe GA (2001) Genetic analysis of wound signaling in tomato. Evidence for a dual role of jasmonic acid in defense and female fertility. Plant Physiol 127:1414–1417

    Article  PubMed  CAS  Google Scholar 

  • Li L, Li C, Lee GI, Howe GA (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci USA 99:6416–6421

    Article  PubMed  CAS  Google Scholar 

  • Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J, Whalon ME, Pichersky E, Howe GA (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16:126–143

    Article  PubMed  CAS  Google Scholar 

  • Li C, Schilmiller AL, Liu G, Lee GI, Jayanty S, Sageman C, Vrebalov J, Giovannoni JJ, Yagi K, Kobayashi Y, Howe GA (2005) Role of beta-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17:971–986

    Article  PubMed  CAS  Google Scholar 

  • Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2. doi:10.1126/scisignal.2000448

  • Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80

    Article  PubMed  CAS  Google Scholar 

  • Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895–897

    Article  PubMed  CAS  Google Scholar 

  • Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377

    Article  PubMed  CAS  Google Scholar 

  • Sembdner G, Parthier B (1993) The biochemistry and the physiological and molecular actions of jasmonates. Annu Rev Plant Physiol Plant Mol Biol 44:569–589

    Article  CAS  Google Scholar 

  • Staswick PE (2008) JAZing up jasmonate signaling. Trends Plant Sci 13:66–71

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89:6837–6840

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE, Tiryaki I, Rowe ML (2002) Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14:1405–1415

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE, 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  CAS  Google Scholar 

  • Suza WP, Staswick PE (2008) The role of JAR1 in jasmonoyl-l-isoleucine production during Arabidopsis wound response. Planta 227:1221–1232

    Article  PubMed  CAS  Google Scholar 

  • Terol J, Domingo C, Talón M (2006) The GH3 family in plants: genome wide analysis in rice and evolutionary history based on EST analysis. Gene 371:279–290

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tiryaki I, Staswick PE (2002) An Arabidopsis mutant defective in jasmonate response is allelic to the auxin-signaling mutant axr1. Plant Physiol 130:887–894

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Halitschke R, Kang JH, Berg A, Harnisch F, Baldwin IT (2007) Independently silencing two JAR family members impairs levels of trypsin proteinase inhibitors but not nicotine. Planta 226:159–167

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, Wang Z, Xie D (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21:2220–2236

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank G. Howe for providing the jai1 mutant and for helpful discussions. We also acknowledge the expertise of T. Clemente and the University of Nebraska Transformation Facility for providing the tomato transformants. This research is a contribution of the University of Nebraska Agricultural Research Division, supported in part by funds from the Hatch Act. Additional support was provided by the National Science Foundation (Awards MCB-0130868, IOS-0744758).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul E. Staswick.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 367 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suza, W.P., Rowe, M.L., Hamberg, M. et al. A tomato enzyme synthesizes (+)-7-iso-jasmonoyl-l-isoleucine in wounded leaves. Planta 231, 717–728 (2010). https://doi.org/10.1007/s00425-009-1080-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-009-1080-6

Keywords

Navigation