Abstract
In response to insect feeding, corn plants (Zea mays cv. Delprim) release elevated levels of volatile organic compounds (VOCs), including the C6-volatile (Z)-3-hexenol. The level of mRNA accumulation for a series of defense genes was monitored in response to application of (Z)-3-hexenol (50 nmol) to undamaged plants. The induction of transcripts for hpl (hydroperoxide lyase), fps (farnesyl pyrophosphate synthase), pal (phenylalanine ammonia-lyase), lox (lipoxygenase), igl (indole-3-glycerol phosphate lyase) and mpi (maize proteinase inhibitor) were compared with metabolites generated from the respective pathways. While headspace VOC analysis showed an increase in (Z)-3-hexenyl acetate and methyl salicylate with lox and pal induction, respectively, MPI accumulation was not observed with an increase in mpi transcripts. Moreover, (Z)-3-hexenol treatment did not elevate sesquiterpene emissions or activate fps transcription. Chemical labeling and bioassay experiments established that exogenous (Z)-3-hexenol can be taken up and converted to a less active acetylated form. These data indicate that (Z)-3-hexenol can serve as a signaling molecule that triggers defense responses in maize and can rapidly be turned over in planta.
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Abbreviations
- BAW :
-
Beet armyworm
- FPS :
-
Farnesyl pyrophosphate synthase
- GAP C :
-
Glycerol phosphate dehydrogenase, cytosolic form
- HMGR :
-
Hydroxymethylglutaryl-coenzyme A reductase
- HPL :
-
Hydroperoxide lyase
- IGL :
-
Indole-3-glycerol phosphate lyase
- LOX :
-
Lipoxygenase
- MeJA :
-
Methyl jasmonate
- MeSA :
-
Methyl salicylate
- MPI :
-
Maize proteinase inhibitor
- PAL :
-
Phenylalanine ammonia lyase
- VOC :
-
Volatile organic compound
References
Alborn HT, Turlings TC, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949
Arimura GI, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000) Herbivory induced volatiles elicit defense genes in lima bean leaves. Nature 406:512–515
Arimura GI, Ozawa R, Horiuchi JI, Nishioka T, Takabayashi J (2001) Plant–plant interactions mediated by volatiles emitted from plants infested by spider mites. Biochem Sys Ecol 29:1049–1061
Bate NJ, Rothstein SJ (1998) C6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J 16:561–569
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–255
Buchanan B, Gruissem W, Jones R (2000) Biochemistry and molecular biology of plants. Wiley, Somerset, NJ, USA
Codero MJ, Raventos D, SanSegundo B (1994) Expression of a maize proteinase inhibitor gene is induced in response to wounding and fungal infection—systemic wound-response of a monocot gene. Plant J 6:141–150
Croft K, Juttner F, Slusarenko AJ (1993) Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiol 101:13–24
Danon A (1997) Translational regulation in the chloroplast. Plant Physiol 115:1293–1298
Doares SH, Narvez-Vasquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108:1741–1746
Engelberth J, Koch TGS, Bachmann N, Rechtenbach J, Boland W (2001) Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling: cross talk between jasmonate and salicylate signaling in lima bean. Plant Physiol 125:369–377
Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1785
Farag MA, Paré PW (2002) C6-green volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61:545–554
Farmer EE (2001) Surface-to-air signals. Nature 411:854–856
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
Frey M, Stettner C, Paré PW, Schmelz E, Tumlinson JH, Gierl A (2000) An herbivore elicitor activates the gene for indole emission in maize. Proc Natl Acad Sci USA 97:14801–14806
Gardener HW, Dornbos DL, Desjardins A (1990) Hexanal, trans-2-hexenal, and trans-2-nonenal inhibit soybean, Glycine max, seed germination. J Agric Food Chem 38:1316–1320
Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19:1720–1730
Ha SB, Lee BC, Lee DE, Kuk YI, Lee Ay, Han OE (2002) Molecular characterization of the gene encoding rice allene oxide synthase and its expression. Biosci Biotechnol Biochem 66:2719–2722
Halitschke R, Kessler A, Klah J, Lorenz A, Baldwin IT (2000) Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuate. Oecologia 124: 408–417
Harms K, Ramirez I, Pena-Cortez H (1998) Inhibition of wound-induced accumulation of allene oxide synthase transcripts in flax leaves by aspirin and salicylic acid. Plant Physiol 118:1057–1065
Hatanaka A, Kajiwara T, Sekiya J (1987) Biosynthesis pathway for C6-aldehydes formation from linolenic acid in green leaves. Chem Phys Lipids 44:341–361
Hildebrand DF, Hamilton-Kemp TR, Legg CS, Bookjans G (1988) Plant lipoxygenase: occurrence, properties and possible functions. Plant Biochem Physiol 7:201–219
Hildebrand DF, Brown GC, Jackson DM, Hamilton TR (1993) Effect of some leaf emitted volatiles compounds on aphid population increase. J Chem Ecol 19:1875–1887
Hoffman T, Schmidt J, Zheng X, Bent A (1999) Isolation of ethylene insensitive soybean mutants that are altered in pathogen susceptibility and gene-for-gene resistance. Plant Physiol 119:935–949
Keinänen M, Oldham NJ, Baldwin IT (2001) Rapid HPLC screening of jasmonate-induced increases in tobacco alkaloids, phenolics, and diterpene glycosides in Nicotiana attenuata. J Agric Food Chem 49:3553–3558
Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2143
Kim ES, Back K, Baik M, Choi E, Han O (2001) Sequence of the wound-responsive lipoxygenase gene from maize plants. J Biochem Mol Biol 34:259–261
Kim ES, Kim EH, Park RD, Lee Y, Han O (2002) Dual positional specificity of wound-responsive lipoxygenase from maize plants. J Plant Physiol 159:1263–1265
King EG, Leppla NC (1984) Advances and challenges in insect rearing. US Government Printing Services, Washington, DC
Koch T, Bandemer K, Boland W (1997) Biosynthesis of cis-jasmone: a pathway for the inactivation and the disposal of the plant stress hormone jasmonic acid to the gas phase. Helv Chem Acta 80:838–850
Koch T, Krumm T, Jung V, Engelberth J, Boland W (1999) Differential Induction of plant volatile biosynthesis in the lima bean by early and late intermediates of the octadecanoid-signaling pathway. Plant Physiol 121:153–162
Kohlmann M, Bachmann A, Weichert H, Kolbe A, Balkenhohl T, Wasternack C, Feussner I (1999) Formation of lipoxygenase-pathway-derived aldehydes in barley leaves upon methyl jasmonate treatment. Eur J Biochem 260:885–895
Martin DM, Gershenzon J, Bohlmann J (2003) Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiol 132:1586–1599
Paré PW, Tumlinson JH (1997) De novo biosynthesis of volatiles induced by insect herbivore in cotton plants. Plant Physiol 114:1161–1167
Paré PW, Tumlinson JH (1998) Cotton volatiles synthesized and released distal to the site of insect damage. Phytochemistry 47:521–526
Paré PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–331
Rao MV, Lee H, Creelman RA, Mullet JE, Davis KR (2000) Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12:1633–1646
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, vol 3, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
Saona CR, Craft SJ, Paré PW, Henneberry TJ (2001) Exogenous methyl jasmonate induces volatile emissions in cotton plants. J Chem Ecol 27:679–695
Schmelz EA, Engelberth J, Alborn HT, O’Donnell P, Sammons M, Toshima H, Tumlinson JH (2003a) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc Natl Acad Sci USA 100:10552–10557
Schmelz EA, Alborn HT, Engelberth J, Tumlinson JH (2003b) Nitrogen deficiency increases volicitin-induced volatile emission, jasmonic acid accumulation, and ethylene sensitivity in maize. Plant Physiol 133:295–306
Shulaev V, Silverman P, Raskin I (1997) Airborne signaling by methyl salicylate in plant pathogen resistance. Nature 385:718–721
Sivasankar S, Sheldrick B, Rothstein SJ (2000) Expression of allene oxide synthase determines defense gene activation in tomato. Plant Physiol 122:1335–1342
Tamayo MC, Rufat M, Bravo JM, San Segund B (2000) Accumulation of a maize proteinase inhibitor in response to wounding and insect feeding, and characterization of its activity toward digestive proteinases of Spodoptera littoralis larvae. Planta 211:62–71
Thaler JS (1999) Jasmonate-inducible plant defenses cause increased parasitism of herbivores. Nature 399:686–688
Thaler JS, Farag MA, Paré PW, Dicke M (2002) Jasmonate-deficient plants have reduced direct and indirect defenses against herbivores. Ecol Lett 5:764–774
Turlings TC, Tumlinson JH (1992) Systemic release of chemical signals by herbivore-injured corn. Proc Natl Acad Sci USA 89:8399–8402
Truitt CL, Wei HX, Paré PW (2004) A plasma membrane protein from Zea mays binds with the herbivore elicitor volicitin. Plant Cell 16:523–532
Weidhase RA, Kramell HM, Lehmann J, Leibisch HW, Lerbs W, Parthier B (1987) Methyl jasmonate-induced changes in the polypeptide pattern of senescing barley leaf segments. Plant Sci 51:177–186
Xu T, Zhou Q, Chen W, Zhang GR, He GF, Gu DX, Zhang WQ (2003) Involvement of jasmonate signaling pathway in the herbivore induced rice plant defense. Chin Sci Bull 48:1982–1987
Zeringue HJ (1992) Effects of C6-C10 alkenals and alkanals on eliciting a defense response in the developing cotton ball. Phytochemistry 3:2305–2308
Acknowledgements
We thank Blanca San Segundo for kindly providing the MPI antibody. This work was supported in part by the U.S. Department of Agriculture (grant no. 35320-9378), by the Herman Frasch Foundation for Chemical Research, and by the Robert A. Welch Foundation (grant no. D-478).
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Farag, M.A., Fokar, M., Abd, H. et al. (Z)-3-Hexenol induces defense genes and downstream metabolites in maize. Planta 220, 900–909 (2005). https://doi.org/10.1007/s00425-004-1404-5
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DOI: https://doi.org/10.1007/s00425-004-1404-5