Skip to main content
SpringerLink
Log in

Genomic Analysis of the 12-oxo-phytodienoic Acid Reductase Gene Family of Zea mays

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The 12-oxo-phytodienoic acid reductases (OPRs) are enzymes that catalyze the reduction of double bonds adjacent to an oxo group in α,β-unsaturated aldehydes or ketones. Some of them have very high substrate specificity and are part of the octadecanoid pathway which convert linolenic acid to the phytohormone jasmonic acid (JA). Sequencing and analysis of ESTs and genomic sequences from available private and public databases revealed that the maize genome encodes eight OPR genes. Southern blot analysis and mapping of individual OPR genes to maize chromosomes using oat maize chromosome addition lines provides independent confirmation of this number of OPR genes in maize. A survey of massively parallel signature sequencing (MPSS) assays revealed that transcripts of each OPR gene accumulate differentially in diverse organs of maize plants suggesting distinct biological functions. Similarly, RNA blot analysis revealed that distinct OPR genes are differentially regulated in response to stress hormones, wounding or pathogen infection. ZmOPR1 and/or ZmOPR2 appear to function in defense responses to pathogens because they are transiently induced by salicylic acid (SA), chitooligosaccharides, and by infection with Cochliobolus  carbonum, Cochliobolus  heterostrophus and Fusarium  verticillioides, but not by wounding. In contrast to these two genes, transcript levels of ZmOPR6 and ZmOPR7 and/or ZmOPR8 are highly induced by wounding or treatments with the wound-associated signaling molecules JA, ethylene and abscisic acid. However, accumulation of ZmOPR6 and ZmOPR7/8 mRNAs was not upregulated by SA treatments or by pathogen infection suggesting specific involvement in the wound-induced defense responses. None of the treatments induced transcripts of ZmOPR3, 4, or 5.

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

Similar content being viewed by others

References

  • G.K. Agrawal N.S. Jwa J. Shibato O. Han H. Iwahashi R. Rakwal (2003) ArticleTitleDiverse environmental cues transiently regulate OsOPR1 of the “octadecanoid pathway” revealing its importance in rice defense/stress and development Biochem. Biophys. Res. Commun. 310 1073–1082 Occurrence Handle10.1016/j.bbrc.2003.09.123 Occurrence Handle14559225

    Article  PubMed  Google Scholar 

  • G.K. Agrawal S. Tamogami O. Han H. Iwahashi R. Rakwal (2004) ArticleTitleRice octadecanoid pathway Biochem. Biophys. Res. Commun. 317 1–15 Occurrence Handle10.1016/j.bbrc.2004.03.020 Occurrence Handle15047141

    Article  PubMed  Google Scholar 

  • E.V. Ananiev O. Riera-Lizarazu H.W. Rines R.L. Phillips (1997) ArticleTitleOat-maize chromosome addition lines: a new system for mapping the maize genome Proc. Natl. Acad. Sci. U.S.A. 94 3524–3529 Occurrence Handle10.1073/pnas.94.8.3524 Occurrence Handle9108009

    Article  PubMed  Google Scholar 

  • C. Biesgen E.W. Weiler (1999) ArticleTitleStructure and regulation of OPR1 and OPR2, two closely related genes encoding 12-oxophytodienoic acid-10,11-reductases from Arabidopsis Planta 208 155–165 Occurrence Handle10.1007/s004250050545 Occurrence Handle10333582

    Article  PubMed  Google Scholar 

  • S. Brenner M. Johnson J. Bridgham G. Golda D.H. Lloyd D. Johnson S. Luo S. McCurdy M. Foy M. Ewan R. Roth D. George S. Eletr G. Albrecht E. Vermaas S.R. Williams K. Moon T. Burcham M. Pallas R.B. DuBridge J. Kirchner K. Fearon J. Mao K. Corcoran (2000) ArticleTitleGene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays Nat. Biotechnol. 18 630–634 Occurrence Handle10.1038/76469 Occurrence Handle10835600

    Article  PubMed  Google Scholar 

  • R.A. Creelman J.E. Mullet (1997) ArticleTitleBiosynthesis and action of jasmonates in plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 355–381 Occurrence Handle10.1146/annurev.arplant.48.1.355 Occurrence Handle15012267

    Article  PubMed  Google Scholar 

  • H. Esterbauer R.J. Schaur H. Zollner (1991) ArticleTitleChemistry and biochemistry of 4-hydroxynonenal, malondialdehyde and related aldehydes Free Rad. Biol. Med. 11 81–128 Occurrence Handle10.1016/0891-5849(91)90192-6 Occurrence Handle1937131

    Article  PubMed  Google Scholar 

  • E.E. Farmer E. Almeras V. Krishnamurthy (2003) ArticleTitleJasmonates and related oxylipins in plant responses to pathogenesis and herbivory Curr. Opin. Plant Biol. 6 372–378 Occurrence Handle10.1016/S1369-5266(03)00045-1 Occurrence Handle12873533

    Article  PubMed  Google Scholar 

  • E.E. Farmer (1994) ArticleTitleFatty acid signaling in plants and their associated microorganisms Plant Mol. Biol. 26 1423–1437 Occurrence Handle10.1007/BF00016483 Occurrence Handle7858198

    Article  PubMed  Google Scholar 

  • E.E. Farmer C.A. Ryan (1990) ArticleTitleInterplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves Proc. Natl. Acad. Sci. U.S.A. 87 7713–7716 Occurrence Handle11607107

    PubMed  Google Scholar 

  • J. Felsenstein (2000) PHYLIP Phylogeny inference package University of Washington Seattle

    Google Scholar 

  • I. Feussner C. Wasternack (2002) ArticleTitleThe lipoxygenase pathway Annu. Rev. Plan Biol. 53 275–297 Occurrence Handle10.1146/annurev.arplant.53.100301.135248

    Article  Google Scholar 

  • B.J. Feys J.E. Parker (2000) ArticleTitleInterplay of signaling pathways in plant disease resistance Trends Genet. 16 449–455 Occurrence Handle10.1016/S0168-9525(00)02107-7 Occurrence Handle11050331

    Article  PubMed  Google Scholar 

  • J.E. Froehlich A. Itoh G.A. Howe (2001) ArticleTitleTomato allene oxide synthase and fatty acid hydroperoxide lyase, two cytochrome P450s involved in oxylipin metabolism, are targeted to different membranes of chloroplast envelope Plant Physiol. 125 306–317 Occurrence Handle10.1104/pp.125.1.306 Occurrence Handle11154338

    Article  PubMed  Google Scholar 

  • G. Haberer T. Hindemitt B.C. Meyers K.F.X. Mayer (2004) ArticleTitleTranscriptional similarities, dissimilarities, and conservation of cis-elements in duplicated genes of Arabidopsis Plant Physiol. 136 3009–3022 Occurrence Handle10.1104/pp.104.046466 Occurrence Handle15489284

    Article  PubMed  Google Scholar 

  • Y. He S. Gan (2001) ArticleTitleIdentical promoter elements are involved in regulation of the OPR1 gene by senescence and jasmonic acid in Arabidopsis Plant Mol. Biol. 47 595–605 Occurrence Handle10.1023/A:1012211011538 Occurrence Handle11725945

    Article  PubMed  Google Scholar 

  • Y. Ishiga A. Funato T. Tachiki K. Toyoda T. Shiraishi T. Yamada Y. Ichinose (2002) ArticleTitleExpression of the 12-oxophytodienoic acid 10,11-reductase gene in the compatible interaction between pea and fungal pathogen Plant Cell Physiol. 43 1210–1220 Occurrence Handle10.1093/pcp/pcf144 Occurrence Handle12407201

    Article  PubMed  Google Scholar 

  • C. Johnson E. Boden J. Arias (2003) ArticleTitleSalicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis Plant Cell 15 1846–1858 Occurrence Handle10.1105/tpc.012211 Occurrence Handle12897257

    Article  PubMed  Google Scholar 

  • J. Kahl D.H. Siemens R.J. Aerts R. Gabler F. Kuhnemann C.A. Preston I.T. Baldwin (2000) ArticleTitleHerbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore Planta 210 336–342 Occurrence Handle10664141

    PubMed  Google Scholar 

  • R. Kohli V. Massey (1998) ArticleTitleThe oxidative half reaction of Old yellow enzyme. The role of tyrosine 196 J. Biol. Chem. 273 32,763–32,770

    Google Scholar 

  • C. Losano Costa P. Arruda C.E. Benedetti (2000) ArticleTitleAn Arabidopsis gene induced by wounding functionally homologous to flavoprotein oxidoreductases Plant Mol. Biol. 44 61–71 Occurrence Handle10.1023/A:1006464822434 Occurrence Handle11094980

    Article  PubMed  Google Scholar 

  • R.A. Martienssen P.D. Rabinowicz A. O’Shaughnessy W.R. McCombie (2004) ArticleTitleSequencing the maize genome Curr. Opin. Plant Biol. 7 102–107 Occurrence Handle10.1016/j.pbi.2004.01.010 Occurrence Handle15003207

    Article  PubMed  Google Scholar 

  • H. Matsui G. Nakamura Y. Ishiga H. Toshima Y. Inagaki K. Toyoda T. Shiraishi Y. Ichinose (2004) ArticleTitleStructure and expression of 12-oxophytodienoate reductase subgroup I. genes in pea, and characterization of the oxidoreductase activities of their recombinant products Mol. Genet. Genomics 271 1–10 Occurrence Handle10.1007/s00438-003-0948-6 Occurrence Handle14727182

    Article  PubMed  Google Scholar 

  • H. Maucher B. Hause I. Feussner J. Ziegler C. Wasternack (2000) ArticleTitleAllene oxide synthases of barley (Hordeum  vulgare cv. Salome): tissue specific regulation in seedling development Plant J. 21 199–213 Occurrence Handle10.1046/j.1365-313x.2000.00669.x Occurrence Handle10743660

    Article  PubMed  Google Scholar 

  • M. McConn R.A. Creelman E. Bell J.E. Mullet J. Browse (1997) ArticleTitleJasmonate is essential for insect defense in Arabidopsis Proc. Natl. Acad. Sci. U.S.A. 94 5473–5477 Occurrence Handle10.1073/pnas.94.10.5473 Occurrence Handle11038546

    Article  PubMed  Google Scholar 

  • S.M. Mount (1982) ArticleTitleA catalogue of splice junction sequences Nucleic Acids Res. 10 459–472 Occurrence Handle7063411

    PubMed  Google Scholar 

  • D.S. Multani R.B. Meeley A.H. Paterson J. Gray S.P. Briggs G.S. Johal (1998) ArticleTitlePlant–pathogen microevolution: molecular basis for the origin of a fungal disease in maize Proc. Natl. Acad. Sci. U.S.A. 95 1686–1691 Occurrence Handle10.1073/pnas.95.4.1686 Occurrence Handle9465077

    Article  PubMed  Google Scholar 

  • R.J. Okagaki R.G. Kynast S.M. Livingston C.D. Russell H.W. Rines R.L. Phillips (2001) ArticleTitleMapping maize sequences to chromosomes using oat-maize chromosome addition materials Plant Physiol. 125 1228–1235 Occurrence Handle10.1104/pp.125.3.1228 Occurrence Handle11244104

    Article  PubMed  Google Scholar 

  • D. Parbery (1996) ArticleTitleTrophism and the ecology of fungi associated with plants Biol. Rev. 71 473–527

    Google Scholar 

  • B. Parthier (1991) ArticleTitleJasmonates, new regulators of plant growth and development: many facts and few hypotheses on their actions Bot. Acta 104 446–454

    Google Scholar 

  • H. Pena-Cortes J. Fisahn L. Willmitzer (1989) ArticleTitleAbscisic acid is involved in the wound-induced expression of the proteinase inhibitor II gene in potato and tomato Proc. Natl. Acad. Sci. U.S.A. 86 9851–9855

    Google Scholar 

  • O. Poirot K. Suhre C. Abergel E. O’Toole C. Notredame (2004) ArticleTitle3DCoffee: a web server for mixing sequences and structures into multiple sequence alignments Nucleic Acids Res. 32 IssueIDWeb Server issue W37–W40 Occurrence Handle10.1093/nar/gnh031 Occurrence Handle15215345

    Article  PubMed  Google Scholar 

  • R. Reekmans K. Smet ParticleDe C. Chen P. Hummelen ParticleVan R. Contreras (2005) ArticleTitleOld yellow enzyme interferes with Bax-induced NADPH loss and lipid peroxidation in yeast FEMS Yeast Res. 5 711–725 Occurrence Handle10.1016/j.femsyr.2004.12.010 Occurrence Handle15851100

    Article  PubMed  Google Scholar 

  • J. Sambrook D.W. Russel (2001) Molecular Cloning: A Laboratory Manual EditionNumber3 Cold Spring Harbor Laboratory Cold Spring Harbor, NY

    Google Scholar 

  • F. Schaller P. Hennig E.W. Weiler (1998) ArticleTitle12-Oxophytodienoate-10,11-reductase: occurrence of two isoenzymes of different specificity against stereoisomers of 12-oxophytodienoic acid Plant Physiol. 118 1345–1351 Occurrence Handle10.1104/pp.118.4.1345 Occurrence Handle9847108

    Article  PubMed  Google Scholar 

  • F. Schaller C. Biesgen C. Mussig T. Altmann E.W. Weiler (2000) ArticleTitle12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis Planta 210 979–984 Occurrence Handle10.1007/s004250050706 Occurrence Handle10872231

    Article  PubMed  Google Scholar 

  • F. Schaller (2001) ArticleTitleEnzymes of the biosynthesis of octadecanoid-derived signalling molecules J. Exp. Bot. 52 11–23 Occurrence Handle10.1093/jexbot/52.354.11 Occurrence Handle11181709

    Article  PubMed  Google Scholar 

  • G.E. Scot S.B. King (1984) ArticleTitleSite of action of factors for resistance to Fusarium moniliforme in maize Plant Dis. 68 804–806

    Google Scholar 

  • D.M. Shah R.C. Hightower R.B. Meagher (1983) ArticleTitleGenes encoding actin in higher plants: intron positions are highly conserved but the coding sequences are not J. Mol. Appl. Genet. 2 111–126 Occurrence Handle6842118

    PubMed  Google Scholar 

  • H. Sobajima M. Takeda M. Sugimori N. Kobashi K. Kiribuchi E.M. Cho C. Akimoto T. Yamaguchi E. Minami N. Shibuya F. Schaller E.W. Weiler T. Yoshihara H. Nishida H. Nojiri T. Omori M. Nishiyama H. Yamane (2003) ArticleTitleCloning and characterization of a jasmonic acid-responsive gene encoding 12-oxophytodienoic acid reductase in suspension-cultured rice cells Planta 216 692–698 Occurrence Handle12569412

    PubMed  Google Scholar 

  • N.M. Springer W.B. Barbazuk (2004) ArticleTitleUtility of different gene enrichment approaches toward identifying and sequencing the maize gene space Plant Physiol. 135 1–11 Occurrence Handle10.1104/pp.900109

    Article  Google Scholar 

  • I. Stenzel B. Hause H. Maucher A. Pitzschke O. Miersch J. Ziegler C.A. Ryan M. Hamberg (1988) ArticleTitleBiosynthesis of 12-oxo-10,15 Z-phytodienoic acid: identification of an allene oxide cyclase Biochem. Biophys. Res. Comm. 156 543–550 Occurrence Handle10.1016/S0006-291X(88)80876-3 Occurrence Handle3178850

    Article  PubMed  Google Scholar 

  • J. Strassner F. Schaller U.B. Frick G.A. Howe E.W. Weiler N. Amrhein P. Macheroux A. Schaller (2002) ArticleTitleCharacterization and cDNA-microarray expression analysis of 12-oxophytodienoate reductases reveals differential roles for octadecanoid biosynthesis in the local versus the systemic wound response Plant J. 32 585–601 Occurrence Handle10.1046/j.1365-313X.2002.01449.x Occurrence Handle12445129

    Article  PubMed  Google Scholar 

  • J. Strassner A. Furholz P. Macheroux N. Amrhein A. Schaller (1999) ArticleTitleA homolog of old yellow enzyme in tomato. Spectral properties and substrate specificity of the recombinant protein J. Biol. Chem. 274 35,067–35,073

    Google Scholar 

  • A. Stintzi J. Browse (2000) ArticleTitleThe Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis Proc. Natl. Acad. Sci. U.S.A. 97 10,625–10,630

    Google Scholar 

  • A. Stintzi H. Weber P. Reymond J. Browse E.E. Farmer (2001) ArticleTitlePlant defense in the absence of jasmonic acid: the role of cyclopentenones Proc. Natl. Acad. Sci. U.S.A. 98 12,837–12,842

    Google Scholar 

  • D.L. Swofford (1998) PAUP*: Phylogenetic Analysis using Parsimony and other Methods Sinauer Associates Sunderland, Mass

    Google Scholar 

  • Swiatek, A., Azmi, A., Witters, E. and van Onckelen, H. 2003. Stress messengers jasmonic acid and abscisic acid negatively regulate plant cell cycleBulg. J. Plant Physiol. Special Issue: 172–178

  • J.S. Thaler B. Owen V.J. Higgins (2004) ArticleTitleThe role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles Plant Physiol. 135 530–538 Occurrence Handle10.1104/pp.104.041566 Occurrence Handle15133157

    Article  PubMed  Google Scholar 

  • B. Thomma I. Penninckx W.F. Broekaert B.P.A. Cammue (2001) ArticleTitleThe complexity of disease signaling in Arabidopsis Curr. Opin. Immunol. 13 63–68 Occurrence Handle10.1016/S0952-7915(00)00183-7 Occurrence Handle11154919

    Article  PubMed  Google Scholar 

  • M.C. Timmermans T.P. Brutnell P.W. Becraft (2004) ArticleTitleThe 46th annual maize genetics conference. Unlocking the secrets of the maize genome Plant Physiol. 136 2633–2640 Occurrence Handle10.1104/pp.104.048702 Occurrence Handle15375208

    Article  PubMed  Google Scholar 

  • J.G. Turner C. Ellis A. Devoto (2002) ArticleTitleThe jasmonate signal pathway Plant Cell 14 S153–S164 Occurrence Handle12045275

    PubMed  Google Scholar 

  • K. Uchida (2003) ArticleTitle4-Hydroxy-2-nonenal: a product and mediator of oxidative stress Prog. Lipid Res. 42 318–343 Occurrence Handle10.1016/S0163-7827(03)00014-6 Occurrence Handle12689622

    Article  PubMed  Google Scholar 

  • B.A. Vick D.C. Zimmerman (1984) ArticleTitleBiosynthesis of jasmonic acid by several plant species Plant Physiol. 75 458–461

    Google Scholar 

  • J. Ziegler I. Stenzel B. Hause H. Maucher M. Hamberg R. Grimm M. Ganal C. Wasternack (2000) ArticleTitleMolecular cloning of allene oxide cyclase: the enzyme establishing the stereochemistry of octadecanoids and jasmonates J. Biol. Chem. 275 19,132–19,138

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Pathology and Microbiology, Department of Plant Pathology, Texas A&M University, 2132 TAMU, College Station, Texas, 77843-2132, USA

    Jinglan Zhang, Heather Wilkinson & Michael Kolomiets

  2. Pioneer Hi-Bred International, Inc., 7250 NW 62nd Ave., Johnston, Iowa, 50131-0552, USA

    Carl Simmons, Nasser Yalpani & Virginia Crane

Authors
  1. Jinglan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carl Simmons
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nasser Yalpani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Virginia Crane
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Heather Wilkinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michael Kolomiets
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael Kolomiets.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, J., Simmons, C., Yalpani, N. et al. Genomic Analysis of the 12-oxo-phytodienoic Acid Reductase Gene Family of Zea mays. Plant Mol Biol 59, 323–343 (2005). https://doi.org/10.1007/s11103-005-8883-z

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-005-8883-z

Keywords

Search

Navigation