Skip to main content
SpringerLink
Log in

The Maize An2 Gene is Induced by Fusarium Attack and Encodes an ent-Copalyl Diphosphate Synthase

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Using the technique of differential display, a maize transcript was identified whose silk tissue expression is induced in the presence of the ear rot pathogen Fusarium graminearum. The 3445 nt transcript includes a 727 nt 5′ untranslated leader with the potential for extensive secondary structure and represents the maize gene An2. An2 encodes a copalyl diphosphate synthase (CPS)-like protein with 60% amino acid sequence identity with the maize An1 gene product involved in gibberellin (GA) biosynthesis. Recombinant expression and functional analysis demonstrated that both AN1 and AN2 are ent-copalyl diphosphate (ent-CPP) synthases (ent-CPS). Notably, the presence of an additional ent-CPS gene is consistent with previous reports that maize GA biosynthesis can proceed in the absence of An1. In addition, northern blot analysis showed that An2 transcript levels were strongly up-regulated by Fusarium attack, with an increase in silk, husk and ear tip tissues as early as 6 h after inoculation of silk channels with spore suspensions of various Fusarium sp. Gene expression of a third maize CPS-like gene, Cpsl1, is not affected by Fusarium infection. The Fusarium-inducible nature of An2 is also consistent with a previous report that cell-free extracts from maize seedlings produce ent-CPP derived diterpenes in response to Fusarium infection. However, it is not known whether An2 is involved in defense-related secondary metabolism in addition to GA synthesis.

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

Abbreviations

CPP:

copalyl diphosphate

CPS:

copalyl diphosphate synthase

DD:

differential display

Fg:

Fusarium graminearum

GA:

gibberellin

GC–MS:

gas chromatography–mass spectrometry

GGPP:

geranylgeranyl diphosphate

GST:

glutathione S-transferase

References

  • B. Bailey-Serres (1999) ArticleTitleSelective translation of cytoplasmic mRNAs in plants Trends Plant Sci. 4 142–148 Occurrence Handle10.1016/S1360-1385(99)01386-2 Occurrence Handle10322548

    Article  PubMed  Google Scholar 

  • R.J. Bensen G.S. Johal V.C. Crane J.T. Tossberg P.S. Schnable R.B. Meeley S.P. Briggs (1995) ArticleTitleCloning and characterization of the maize An1 gene Plant Cell 7 75–84 Occurrence Handle10.1105/tpc.7.1.75 Occurrence Handle7696880 Occurrence Handle1:CAS:528:DyaK2MXjsVyjsbs%3D

    Article  PubMed  CAS  Google Scholar 

  • Briggs, S.P. and Bensen, R.J. 1998. Plant Genes Affecting Gibberellic Acid Biosynthesis. U.S. patent #5773288, Published June 30:1998

  • D. Callard B. Lescure L. Mazzolini (1994) ArticleTitleA method for the elimination of false positives generated by the mRNA differential display technique Biotechniques 16 1096–1103 Occurrence Handle7521188 Occurrence Handle1:CAS:528:DyaK2MXhs1KktA%3D%3D

    PubMed  CAS  Google Scholar 

  • D.W. Cartwright P. Langcake R.J. Pryce D.P. Leworthy J.P. Ride (1977) ArticleTitleChemical activation of host defence mechanisms as a basis for crop protection Nature 267 511–513 Occurrence Handle10.1038/267511a0 Occurrence Handle1:CAS:528:DyaE2sXlt1ymu7k%3D

    Article  CAS  Google Scholar 

  • J. Chappell (1995) ArticleTitleBiochemistry and molecular biology of the isoprenoid biosynthesic pathway in plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 46 521–547 Occurrence Handle10.1146/annurev.pp.46.060195.002513 Occurrence Handle1:CAS:528:DyaK2MXmsVCquro%3D

    Article  CAS  Google Scholar 

  • J. Chappell R. Nable (1987) ArticleTitleInduction of sesquiterpenoid biosynthesis in tobacco cell suspension cultures by fungal elicitor Plant Physiol. 85 469–473 Occurrence Handle1:CAS:528:DyaL2sXmtlegsrg%3D Occurrence Handle16665722

    CAS  PubMed  Google Scholar 

  • E.-M. Cho A. Okada H. Kenmoku K. Otomo T. Toyomasu W. Mitsuhashi T. Sassa A. Yajima G. Yabuta K. Mori (2004) ArticleTitleMolecular cloning and characterization of a cDNA encoding ent-cassa-12,15-diene synthase, a putative diterpenoid phytoalexin biosynthetic enzyme, from suspension-cultured rice cells treated with a chitin elicitor Plant J. 37 1–8 Occurrence Handle10.1046/j.1365-313X.2003.01926.x Occurrence Handle14675427 Occurrence Handle1:CAS:528:DC%2BD2cXptFKnuw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • J.D. Duncan C.A. West (1981) ArticleTitleProperties of kaurene synthetase from Marah macrocarpus endosperm: Evidence for the participation of separate but interacting enzymes Plant Physiol. 68 1128–1134 Occurrence Handle1:CAS:528:DyaL38Xhs1Ghsg%3D%3D Occurrence Handle16662063

    CAS  PubMed  Google Scholar 

  • M. Essenberg M.L. Pierce E.C. Cover B. Hamilton P.E. Richardson V.E. Scholes (1992) ArticleTitleA method for determining phytoalexin concentrations in fluorescent, hypersensitively necrotic cells in cotton leaves Physiol. Mol. Plant Pathol. 41 101–109 Occurrence Handle1:CAS:528:DyaK3sXhs1CntLg%3D

    CAS  Google Scholar 

  • R. Hammerschmidt (1999) ArticleTitlePhytoalexins: What have we learned after 60 years? Annu. Rev. Phytopathol. 37 285–306 Occurrence Handle10.1146/annurev.phyto.37.1.285 Occurrence Handle11701825 Occurrence Handle1:CAS:528:DyaK1MXnt1Wnt7o%3D

    Article  PubMed  CAS  Google Scholar 

  • P. Hedden A.L. Phillips (2000) ArticleTitleGibberellin metabolism: New insights revealed by the genes Trends Plant Sci. 5 523–530 Occurrence Handle10.1016/S1360-1385(00)01790-8 Occurrence Handle11120474 Occurrence Handle1:STN:280:DC%2BD3M7gvVentQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • C.P. Joshi H. Zhou X. Huang V.L. Chiang (1997) ArticleTitleContext sequences of translation initiation codon in plants Plant Mol. Biol. 35 993–1001 Occurrence Handle10.1023/A:1005816823636 Occurrence Handle9426620 Occurrence Handle1:CAS:528:DyaK1cXis1Krsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • M. Katsumi (Eds) (1964) Gibberellin-like activities of certain auxins and diterpenes University of California Los Angeles

    Google Scholar 

  • M. Kozak (1991) ArticleTitleAn analysis of vertebrate mRNA sequences: Intimations of translational control J. Cell Bio. 115 887–903 Occurrence Handle1:CAS:528:DyaK3MXmsV2jtL0%3D

    CAS  Google Scholar 

  • J. Lacey N. Magan (1991) Fungi in cereal grains: Their occurrence and water and temperature relationships J. Chelkowski (Eds) Cereal Grain: Mycotoxins, Fungi and Quality in Drying and Storage Elsevier Science Publ Poland 77–118

    Google Scholar 

  • T. Lange (1998) ArticleTitleMolecular biology of gibberellin synthesis Planta 204 409–419 Occurrence Handle9684365 Occurrence Handle1:CAS:528:DyaK1cXitVOmtr0%3D

    PubMed  CAS  Google Scholar 

  • P. Liang A.B. Pardee (1992) ArticleTitleDifferential display of eukaryotic messenger RNA by means of the polymerase chain reaction Science 257 967–971 Occurrence Handle1354393 Occurrence Handle1:CAS:528:DyaK38Xls1Cqt70%3D

    PubMed  CAS  Google Scholar 

  • S. M. Lohmer Maddaloni M. Motto F. Salamini R.D. Thompson (1993) ArticleTitleTranslation of the mRNA of the maize transcriptional activator Opaque-2 is inhibited by upstream open reading frames present in the leader sequence Plant Cell 5 65–73

    Google Scholar 

  • M. Lukaszewicz M. Feuermann B. Jérouville A. Stas M. Boutry (2000) ArticleTitleIn vivo evaluation of the context sequence of the translation initiation codon in plants Plant Sci. 154 89–98 Occurrence Handle10.1016/S0168-9452(00)00195-3 Occurrence Handle10725562 Occurrence Handle1:CAS:528:DC%2BD3cXhvV2mtLs%3D

    Article  PubMed  CAS  Google Scholar 

  • D.H. Mathews J. Sabina M. Zuker D.H. Turner (1999) ArticleTitleExpanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure J. Mol. Biol. 288 911–940 Occurrence Handle10.1006/jmbi.1999.2700 Occurrence Handle10329189 Occurrence Handle1:CAS:528:DyaK1MXjtVers7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • M. McMullen R. Jones D. Gallenberg (1997) ArticleTitleScab of wheat and barley: A re-emerging disease of devastating impact Plant Disease 81 1340–1348

    Google Scholar 

  • J.E. Mellon C.A. West (1979) ArticleTitleDiterpene biosynthesis in maize seedlings in response to fungal infection Plant Physiol. 64 406–410 Occurrence Handle1:CAS:528:DyaE1MXlslWrs7Y%3D Occurrence Handle10.1104/pp.64.3.406 Occurrence Handle16660976

    Article  CAS  PubMed  Google Scholar 

  • J.D. Miller (1994) Epidemiology of Fusarium ear diseases of cereals J.D. Miller H.L. Trenholm (Eds) Mycotoxins in Grain: Compounds Other than Aflatoxin Eagan Press St. Paul, Minn 405–419

    Google Scholar 

  • R.S. Mohan N.K.N. Yee R.M. Coates Y.-Y. Ren P. Stamenkovic I. Mendez C.A. West (1996) ArticleTitleBiosynthesis of cyclic diterpene hydrocarbons in rice cell suspensions: Conversion of 9,10-syn-labda-8(17), 13-dienyl diphosphate to 9β-pimara-7,15-diene and stemar-13-ene Arch. Biochem. Biophys. 330 33–47 Occurrence Handle10.1006/abbi.1996.0223 Occurrence Handle8651702 Occurrence Handle1:CAS:528:DyaK28Xjtlaitr4%3D

    Article  PubMed  CAS  Google Scholar 

  • D.W-K. Ng M.B. Chandrasekharan T.C. Hall (2004) ArticleTitleThe 5′ UTR negatively regulates quantitative and spatial expression from the ABI3 promoter Plant Mol. Biol. 54 25–38 Occurrence Handle10.1023/B:PLAN.0000028767.06820.34 Occurrence Handle15159632 Occurrence Handle1:CAS:528:DC%2BD2cXkt1Wjsr4%3D

    Article  PubMed  CAS  Google Scholar 

  • K. Otomo H. Kenmoku H. Oikawa W.A. Konig H. Toshima W. Mitsuhashi H. Yamane T. Sassa T. Toyomasu (2004) ArticleTitleBiological functions of ent- and syn-copalyl diphosphate synthases in rice: Key enzymes for the branchpoint of gibberellin and phytoalexin biosynthesis Plant J. 39 886–893 Occurrence Handle10.1111/j.1365-313X.2004.02175.x Occurrence Handle15341631 Occurrence Handle1:CAS:528:DC%2BD2cXpt1GntLk%3D

    Article  PubMed  CAS  Google Scholar 

  • A.H. Paterson J.E. Bowers B.A. Chapman (2004) ArticleTitleAncient polyploidization predating divergence of the cereals, and its consequences for comparative genomics Proc. Natl. Acad. Sci. USA 101 9903–9908 Occurrence Handle15161969 Occurrence Handle1:CAS:528:DC%2BD2cXlvVahtbY%3D

    PubMed  CAS  Google Scholar 

  • G. Pesole C. Gissi G. Grillo F. Licciulli S. Liuni C. Saccone (2000) ArticleTitleAnalysis of oligonucleotide AUG start codon context in eukaryotic mRNAs Gene 261 85–91 Occurrence Handle10.1016/S0378-1119(00)00471-6 Occurrence Handle11164040 Occurrence Handle1:CAS:528:DC%2BD3MXmvF2mtA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • R.J. Peters R.B. Croteau (2002) ArticleTitleAbietadiene synthase catalysis: conserved residues involved in protonation-initiated cyclization of geranylgeranyl diphosphate to (+)-copalyl diphosphate Biochemistry 41 1836–1842 Occurrence Handle10.1021/bi011879d Occurrence Handle11827528 Occurrence Handle1:CAS:528:DC%2BD38XjtF2rtw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • S Prisic M Xu P.R Wilderman R.J Peters (2004) ArticleTitleRice contains two disparate ent-copalyl diphosphate synthases with distinct metabolic functions Plant Physiol 136 4228–4236 Occurrence Handle10.1104/pp.104.050567 Occurrence Handle15542489 Occurrence Handle1:CAS:528:DC%2BD2MXjtVartg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • L.M. Reid D.E. Mather R.I. Hamilton A.T. Bolton (1992) ArticleTitleGenotypic differences in the resistance of maize silk to Fusarium graminearum Can. J. Plant Pathol. 14 211–214

    Google Scholar 

  • L.M. Reid R.I. Hamilton (1995) ArticleTitleEffect of macroconidial suspension volume and concentration on expression of resistance to Fusarium graminearum in maize Plant Disease 79 461–46 Occurrence Handle10.1094/PD-79-0461

    Article  Google Scholar 

  • Rivin, C.J., Zimmer, E.A. and Walbot, V. 1982. Isolation of DNA and DNA recombinants from maize. In: W.F. Sheridan (Ed.), Maize for Biological Research, Plant Molecular Biology Assoc. pp. 161–164.

  • I.B. Rogozin A.V. Kochetov F.A. Kondrashov E.V. Koonin L. Milanesi (2001) ArticleTitlePresence of ATG triplets in 5′ untranslated regions of eukaryotic cDNAs correlates with a ‘weak’ context of the start codon Bioinformatics 17 890–900 Occurrence Handle10.1093/bioinformatics/17.10.890 Occurrence Handle11673233 Occurrence Handle1:CAS:528:DC%2BD3MXot1Ggtb0%3D

    Article  PubMed  CAS  Google Scholar 

  • T. Sakamoto K. Miura H. Itoh T. Tatsumi M. Ueguchi-Tanaka K. Ishiyama M. Kobayashi G.K. Agrawal S. Takeda K. Abe A. Miyao H. Hirochika H. Kitano M. Ashikari M. Matsuoka (2004) ArticleTitleAn overview of gibberellin metabolism enzyme genes and their related mutants in rice Plant Phys. 134 1642–1653 Occurrence Handle10.1104/pp.103.033696 Occurrence Handle1:CAS:528:DC%2BD2cXjsFKmsb8%3D

    Article  CAS  Google Scholar 

  • W. Spielmeyer M. Ellis M. Robertson S. Ali J.R. Lenton P.M. Chandler (2004) ArticleTitleIsolation of gibberellin metabolic pathway genes from barley and comparative mapping in barley, wheat, and rice Theor. Appl. Genet. 109 847–855 Occurrence Handle15146318 Occurrence Handle1:CAS:528:DC%2BD2cXntFGnsrw%3D

    PubMed  CAS  Google Scholar 

  • K. Vandepoele C. Simillion Y. Peer ParticleVan de (2003) ArticleTitleEvidence that rice and other cereals are ancient aneuploids Plant Cell 15 2192–2202 Occurrence Handle10.1105/tpc.014019 Occurrence Handle12953120 Occurrence Handle1:CAS:528:DC%2BD3sXnsV2gurc%3D

    Article  PubMed  CAS  Google Scholar 

  • H.D. VanEtten J.W. Mansfield J.A. Bailey E.E. Farmer (1994) ArticleTitleTwo classes of plant antibiotics: phytoalexins versus ‘phytoanticipans’ Plant Cell 6 1191–1192 Occurrence Handle10.1105/tpc.6.9.1191 Occurrence Handle12244269 Occurrence Handle1:CAS:528:DyaK2MXpslSqtw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • L. Wang S.R. Wessler (2001) ArticleTitleRole of mRNA secondary structure in translational repression of the maize transcriptional activator Lc Plant Physiol. 125 1380–1387 Occurrence Handle11244117 Occurrence Handle1:CAS:528:DC%2BD3MXitFWrtLc%3D

    PubMed  CAS  Google Scholar 

  • D.C. Williams D.J. McGarvey E.J. Katahira R. Croteau (1998) ArticleTitleTruncation of limonene synthase preprotein provides a fully active ‘pseudomature’ form of this monoterpene cyclase and reveals the function of the amino-terminal arginine pair Biochemistry 37 12213–12220 Occurrence Handle9724535 Occurrence Handle1:CAS:528:DyaK1cXltV2rtro%3D

    PubMed  CAS  Google Scholar 

  • M. Xu M.L. Hillwig S. Prisic R.M. Coates R.J Peters (2004) ArticleTitleFunctional identification of rice syn-copalyl diphosphate synthase and its role in initiating biosynthesis of diterpenoid phytoalexin/allelopathic natural products Plant J. 39 309–318 Occurrence Handle10.1111/j.1365-313X.2004.02137.x Occurrence Handle15255861 Occurrence Handle1:CAS:528:DC%2BD2cXnsVSquro%3D

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Eastern Cereal and Oilseed Research Centre, Agriculture and Agri-Food Canada, Building #21, Central Experimental Farm, K1A 0C6, Ottawa, Ont, Canada

    L. J. Harris, A. Saparno, A. Johnston, S. Allard, A. Kathiresan & T. Ouellet

  2. Department of Biochemistry, Biophysics, and Molecular Biology, Iowa State University, Ames, IA, 50011, USA

    S. Prisic, M. Xu & R. J. Peters

Authors
  1. L. J. Harris
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Saparno
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Johnston
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Prisic
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Allard
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. Kathiresan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. T. Ouellet
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. R. J. Peters
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. J. Harris.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harris, L.J., Saparno, A., Johnston, A. et al. The Maize An2 Gene is Induced by Fusarium Attack and Encodes an ent-Copalyl Diphosphate Synthase. Plant Mol Biol 59, 881–894 (2005). https://doi.org/10.1007/s11103-005-1674-8

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-005-1674-8

Keywords

Search

Navigation