Skip to main content
SpringerLink
Log in

A novel lipoxygenase gene from developing rice seeds confers dual position specificity and responds to wounding and insect attack

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

OsLOX1 is a novel full-length cDNA isolated from developing rice seeds. We have examined its biochemical properties and expression patterns. The protein has dual positional specificity, as it releases both C-9 and C-13 oxidized products in a 4:3 ratio. OsLOX1 transcripts were detected at low abundance in immature seeds and newly germinated seedlings, but accumulate rapidly and transiently in response to wounding or brown planthopper (BPH) attack, reaching a peak 3 h after wounding and 6 h after insect feeding. We produced transgenic rice lines carrying either sense or antisense constructs under the control of a cauliflower mosaic virus 35S promoter, and these rice lines showed altered OsLOX1 activity. In all of the antisense lines and more than half of the sense lines the expression levels of OsLOX1, the levels of enzyme activity, and the levels of the endogenous OsLOX1 products (jasmonic acid, (Z)-3-hexenal and colneleic acid) at 6, 48, and 48 h after BPH feeding respectively, were below the levels found in non-transgenic control plants; yet, the levels in the remaining sense transformants were enhanced relative to controls. Transformants with a lower level of OsLOX1 expression were less able to tolerate BPH attack, while those with enhanced OsLOX1 expression were more resistant. Our data suggest that the OsLOX1 product is involved in tolerance of the rice plant to wounding and BPH attack.

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
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

LOX:

Lipoxygenase

UTR:

Untranslated region

BPH:

Brown planthopper

BTH:

Benzo(1,2,3)thiadiazole-7-carbothioic acid S-methyl ester

CA:

Colneleic acid

ORF:

Open reading frame

JA:

Jasmonic acid

HPOD:

Hydroperoxyoctadecadienoic acid

GFP:

Green fluorescent protein

RACE:

Rapid amplification of cDNA end

HPLC:

High performance liquid chromatography

References

  • Alam SN, Cohen MB (1997) Detection and analysis of QTLs for resistance to the brown planthopper, Nilaparvata lugens, in a doubled-haploid rice population. Theor Appl Genet 97:1370–1379

    Article  Google Scholar 

  • Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949

    Article  CAS  Google Scholar 

  • Anderson JM (1989) Membrane derived fatty acids as precursors to second messengers. In: Boss WF, Morre DJ (eds) Second messengers in plant growth and development, vol 6. Alan R. Liss, New York, pp 181–212

    Google Scholar 

  • Chen GP, Hackett R, Walker D, Taylor A, Lin ZF, Grierson D (2004) Identification of a specific isoform of tomato lipoxygenase (TomloxC) involved in the generation of fatty acid-derived flavor compounds. Plant Physiol 136:2641–2651

    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 

  • Feussner I, Wasternack C (1998) Lipoxgenase catalyzed oxygenation of lipids. Fett-lipid 100:146–152

    Article  CAS  Google Scholar 

  • Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol Physiol Plant Mol Biol 53:275–279

    CAS  Google Scholar 

  • Fukuchi-Mizutani M, Ishiguro K, Nakayama T, Utsunomiya Y, Tanaka Y, Kusumi T, Ueda T (2000) Molecular and functional characterization of a rose lipoxygenase cDNA related to flower senescence. Plant Sci 160:129–137

    Article  PubMed  CAS  Google Scholar 

  • Fuse T, Sasaki T, Yano M (2001) Ti-plasmid vectors useful for functional analysis of rice genes. Plant Biotechnol 18:219–222

    CAS  Google Scholar 

  • Göbel C, Feussner I, Rosahl S (2003) Lipid peroxidation during the hypersensitive response in potato in the absence of 9-lipoxygenase. J Biol Chem 278(52):52834–52840

    Article  PubMed  CAS  Google Scholar 

  • Halitschke R, Baldwin IT (2003) Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuate. Plant J 36:794–807

    Article  PubMed  CAS  Google Scholar 

  • Höhne M, Nellen A, Schwennesen K, Kindl H (1996) Lipid body lipoxygenase characterized by protein fragmentation, cDNA sequence and very early expression of the enzyme during germination of cucumber seeds. Eur J Biochem 241:6–11

    Article  PubMed  Google Scholar 

  • Holsters M, De Waele D, Depicker A, Messens E, Van Montagu M, Schell J (1978) Transfection and transformation of Agrobacterium tumefaciens. Mol Gen Genet 163:181–187

    Article  PubMed  CAS  Google Scholar 

  • Hornung E, Walther M, Kühn H, Feussner I (1999) Conversion of cucumber linoleate 13-lipoxygenase to a 9-lipoxygenating species by sitedirected mutagenesis. Proc Natl Acad Sci USA 96:4192–4197

    Article  PubMed  CAS  Google Scholar 

  • Huang Z, He G, Shu L, Li X, Zhang Q (2001) Identification and mapping of two brown planthopper resistance genes in rice. Theor Appl Genet 102:929–934

    Article  CAS  Google Scholar 

  • Hughes RK, Wu Z, Robinson DS, Hardy D, West SI, Fairhurst SA, Casey R (1998) Characterization of authentic recombinant pea-seed lipoxygenases with distinct properties and reaction mechanisms. Biochem J 333:33–43

    PubMed  CAS  Google Scholar 

  • Hughes RK, West SI, Hornostaj AR, Lawson DM, Fairhurst SA, Sanchez RO, Hough P, Robinson BH, Casey R (2001) Probing a novel potato lipoxygenase with dual positional specificity reveals primary determinants of substrate binding and requirements for a surface hydrophobic loop and has implications for the role of lipoxygenases in tubers. Biochem J 353:345–355

    Article  PubMed  CAS  Google Scholar 

  • Ida S, Masaki Y, Morita Y (1983) The isolation of multiple forms and product specificity of rice lipoxygenase. Agric Biol Chem 47:637–641

    CAS  Google Scholar 

  • Ishii T, Brar DS, Multani DS, Khush GS (1994) Molecular tagging of genes for brown planthopper resistance and earliness introgressed from Oryza australiensis into cultivated rice, O. sativa. Genome 37:217–221

    CAS  PubMed  Google Scholar 

  • Kim ES, Choi E, Kim Y, Cho K, Lee A, Shim J, Rakwal R, Agrawal GK, Han O (2003) Dual positional specificity and expression of non-traditional lipoxygenase induced by wounding and methyl jasmonate in maize seedlings. Plant Mol Biol 52:1203–1213

    Article  PubMed  Google Scholar 

  • Knox M, Forster C, Domoney C, Casey R (1994) Structure of the Pisum sativum seed lipoxygenase gene lox1:Ps:3. Biochim Biophys Acta 1214:341–343

    PubMed  Google Scholar 

  • Kolomiets MV, Chen H, Gladon RJ, Braun EJ, Hannapel DJ (2000) A leaf lipoxygenase of potato induced specifically by pathogen infection. Plant Physiol 124:1121–1130

    Article  PubMed  CAS  Google Scholar 

  • Ling KC (1972) Rice virus diseases. International Rice Research Institute, Las Banos, Philippines, pp 11–33

    Google Scholar 

  • Lou YG, Cheng JA, Ping XF, Tang FB, Ru SJ, Du MH (2002) Discrimination by the egg parasitoid Anagrus nilaparvatae between two hosts, Nilaparvata lugens and Sogatella furcifera. Acta Entomol Sin 45:770–776

    CAS  Google Scholar 

  • Ma JF, Goto S, Tamai K, Ichii M (2001) Role of root hairs and lateral roots in silicon uptake by rice. Plant Physiol 127:1773–1780

    Article  PubMed  CAS  Google Scholar 

  • Ma S, Quist TM, Ulanov A, Joly R, Bohnert HJ (2004) Loss of TIP1;1 aquaporin in Arabidopsis leads to cell and plant death. Plant J 40:845–859

    Article  PubMed  CAS  Google Scholar 

  • McConn M, Creelman RA, Bell E, Mullet JE, Browse J (1997) Jasmonate is essential for insect defense in Arabidopsis. Proc Natl Acad Sci USA 94:5473–5477

    Article  PubMed  CAS  Google Scholar 

  • Mizuno K, Iida T, Takano A, Yokoyama M, Fujimura T (2003) A new 9-lipoxygenase cDNA from developing rice seeds. Plant Cell Physiol 44:1168–1175

    Article  PubMed  CAS  Google Scholar 

  • Moran PJ, Thompson GA (2001) Molecular responses to Aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol 125:1074–1085

    Article  PubMed  CAS  Google Scholar 

  • Nemchenko A, Kunze S, Feussner I, Kolomiets M (2006) Duplicate maize 13-lipoxygenase genes are differentially regulated by circadian rhythm, cold stress, wounding, pathogen infection, and hormonal treatments. J Exp Bot 57:3767–3779

    Article  PubMed  CAS  Google Scholar 

  • Ongena M, Dubby F, Rossignol F, Fauconnier ML, Dommes J, Thonart P (2004) Stimulation of the lipoxygenase pathyway is associated with systemic resistance induced in bean by a nonpathogenic Pseudomonas strain. Mol Plant Microbe Int 17:1009–1018

    Article  CAS  Google Scholar 

  • Ohta H, Ida S, Mikami B, Morita Y (1986) Changes in lipoxygenase components of rice seedlings during germination. Plant Cell Physiol 27:911–918

    CAS  Google Scholar 

  • Ohta H, Shirano Y, Tanaka K, Morita Y, Shibata D (1992) cDNA cloning of rice lipoxygenase L-2 and characterization using an active enzyme expressed from the cDNA in Escherichia coli. Eur J Biochem 206:331–336

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Brubaker CL, Wendel JF (1993) A rapid method for extraction of cotton genomic DNA suitable for RFL P and PCR analysis. Plant Mol Biol Rep 11:122–127

    CAS  Google Scholar 

  • Pathak MD, Cheng CH, Fortuno ME (1969) Resistance to Nephotettix impictiveps and Nilaparvata lugens in varieties of rice. Nature 223:502–504

    Article  Google Scholar 

  • Peng Y, Shirano Y, Ohta H, Hibino T, Tanaka K, Shibata D (1994) A novel lipoxygenase from rice. Primary structure and specific expression upon incompatible infection with rice blast fungus. J Biol Chem 269:3755–3761

    PubMed  CAS  Google Scholar 

  • Porta H, Rocha-Sosa M (2002) Plant lipoxygenases. Physiological and molecular features. Plant Physiol 130:15–21

    Article  PubMed  CAS  Google Scholar 

  • Reece KS, McElroy D, Wu R (1990) Genomic nucleotide sequence of four rice (Oryza sativa) actin genes. Plant Mol Biol 14:621–624

    Article  PubMed  CAS  Google Scholar 

  • Rosahl S (1996) Lipoxygenases in plants. Their role in development and stress response. Z Naturforsch 51:123–138

    CAS  Google Scholar 

  • Royo J, Vancanneyt G, Pérez AG, Sanz C, Störmann K, Rosahl S, Sánchez-Serrano JJ (1996) Characterization of three potato lipoxygenases with distinct enzymatic activities and different organ-specific and wound-regulated expression patterns. J Biol Chem 271:21012–21019

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd ed. Cold-Spring Harbor Laboratory Press, Cold Spring harbor, NY

    Google Scholar 

  • Santino A, Iannacone R, Hughes R, Casey R, Mita G (2005) Cloning and characterization of an almond 9-lipoxygenase expressed early during seed development. Plant Sci 168:699–706

    Article  CAS  Google Scholar 

  • Schaffrath U, Zabbai F, Dudler R (2000) Characterization of RCI-1, a chloroplastic rice lipoxygenase whose synthesis is induced by chemical plant resistance activators. Eur J Biochem 267:5935–5942

    Article  PubMed  CAS  Google Scholar 

  • Schweizer P, Buchala A, Silverman P, Sesker M, Baskin I, Metraux JP (1997) Jasmonate-inducible genes are activated in rice by pathogen attack without a concomitant increase in endogenous jasmonic acid levels. Plant Physiol 114:79–88

    PubMed  CAS  Google Scholar 

  • Schweizer P, Buchala A, Dudler R, Metraux JP (1998) Induced systemic resistance in wounded rice plants. Plant J 14:475–481

    Article  CAS  Google Scholar 

  • Sheen J (2002a) Phosphorelay and transcription control in cytokinin signal transduction. Science 296:1650–1652

    Article  PubMed  CAS  Google Scholar 

  • Sheen J (2002b) A transient expression assay using Arabidopsis mesophyll protoplasts. Massachusetts General Hospital Department of Molecular Biology Genetics Web Server. http://www.genetics.mgh.harvard.edu/sheenweb/protocols.html. (May 28, 2007)

  • Shibata D, Slusarenko A, Casey R, Hildebrand D, Bell E (1994) Lipoxygenase. Plant Mol Biol Rep 12:S41–S42

    Article  CAS  Google Scholar 

  • Shibata D, Steczko J, Dixon JE, Andrews PC, Hermodson M, Axelrod B (1988) Primary structure of soybean lipoxygenase-2. J Biol Chem 263:6816–6821

    PubMed  CAS  Google Scholar 

  • Siedow JN (1991) Plant lipoxygenases: structure and functions. Annu Rev Plant Physiol Plant Mol Biol 42:145–188

    Article  CAS  Google Scholar 

  • Sofo A, Dichio B, Xiloyannis C, Masia A (2004) Lipoxygenase activity and praline accumulation in leaves and roots of olive trees in response to drought stress. Physiol Plantarum 121:58–65

    Article  CAS  Google Scholar 

  • Suzuki Y, Matsukura U (1997) Lipoxygenase activity in maturing and germinating rice seeds with and without lipoxygenase-3 in mature seeds. Plant Sci 125:119–126

    Article  CAS  Google Scholar 

  • Thaler J (1999) Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686–688

    Article  CAS  Google Scholar 

  • Vijayan P, Shockey J, Lévesque CA, Cook RJ, Browse J (1998) A role for jasmonate in pathogen defense of Arabidopsis. Proc Natl Acad Sci USA 95:7209–7214

    Article  PubMed  CAS  Google Scholar 

  • van Loon LC (1997) Induced resistance in plants and the roles of pathogenesis-related proteins. Eur J Plant Pathol 103:753–765

    Article  Google Scholar 

  • van Mechelen JR, Schuurink RC, Smits M, Graner A, Douma AC, Sedee NJ, Schmitt NF, Valk BE (1999) Molecular characterization of two lipoxygenases from barley. Plant Mol Biol 39:1283–1298

    Article  PubMed  Google Scholar 

  • Weber H, Chételat A, Caldelari D, Farmer EE (1999) Divinyl ether fatty acid synthesis in late blight-diseased potato leaves. Plant Cell 11:485–493

    Article  PubMed  CAS  Google Scholar 

  • Xu T, Zhou Q, Xia Q, Zhang WQ, Zhang GR, Gu DX (2002) Effects of herbivore-induced rice volatiles on the host selection behavior of brown planthopper, Nilaparvata lugens. Chin Sci Bull 47:1355–1360

    Article  CAS  Google Scholar 

  • Yenofsky RL, Fine M, Liu C (1988) Isolation and characterization of a soybean (Glycine max) lipoxygenase-3 gene. Mol Gen Genet 211:215–222

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key Basic Research “973” Program of China (Grant No. 2004CB117204), by the National “863” program (Grant No. 2006AA100101, 2006AA10Z1A5 and 2006AA10A102), by the National Natural Science Foundation of China (Grant No. 30270817), and by the Program for Changjiang Scholars and Innovative Research Team in University (PCSIRT). We owe special thanks to Prof. Bing Xia and Dr. Yu Shan at Institute of Botany Jiangsu Province & Chinese Academy of Sciences for assaying levels of JA and (Z)-3-hexenal; we also thank Dr. Genji Qin from the College Life Sciences at Peking University for assistance in northern blot analysis, and Prof. Shihu Yang in Nanjing Agricultural University for providing the rice transformation vectors pPZP2Ha3(+) and pPZP2Ha3(-).

Author information

Authors and Affiliations

  1. State Key Laboratory for Crop Genetics & Germplasm Enhancement, Nanjing Agricultural University; Research Center of Plant Gene Engineering, Nanjing, Jiangsu Province, 210095, P. R. China

    Ren Wang, Wenbiao Shen, Linglong Liu, Ling Jiang, Yuqiang Liu & Jianmin Wan

  2. The National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing, 10081, P. R. China

    Ning Su & Jianmin Wan

  3. State Key Laboratory for Crop Genetics & Germplasm Enhancement, Nanjing Agricultural University, Research Institute of Rice, Weigang 1#, Nanjing, Jiangsu Province, 210095, P. R. China

    Jianmin Wan

Authors
  1. Ren Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wenbiao Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Linglong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ling Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuqiang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ning Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jianmin Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jianmin Wan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, R., Shen, W., Liu, L. et al. A novel lipoxygenase gene from developing rice seeds confers dual position specificity and responds to wounding and insect attack. Plant Mol Biol 66, 401–414 (2008). https://doi.org/10.1007/s11103-007-9278-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-007-9278-0

Keywords

Search

Navigation