Theoretical and Applied Genetics

, Volume 114, Issue 5, pp 927–937 | Cite as

Retrotransposon and gene activation in wheat in response to mycotoxigenic and non-mycotoxigenic-associated Fusarium stress

  • Khairul I. Ansari
  • Stephanie Walter
  • Josephine M. Brennan
  • Marc Lemmens
  • Sarah Kessans
  • Angela McGahern
  • Damian Egan
  • Fiona M. Doohan
Original Paper


Despite inhibition of protein synthesis being its mode of action, the trichothecene mycotoxin deoxynivalenol (DON) induced accumulation of transcripts encoding translation elongation factor 1α (EF-1α), class III plant peroxidase (POX), structure specific recognition protein, basic leucine zipper protein transcription factor (bZIP), retrotransposon-like homologs and genes of unknown function in the roots of wheat cultivars CM82036 and Remus. Fusarium head blight (FHB) studies using Fusarium graminearum and its trichothecene-minus (Tri5) mutant derivative and adult plant DON tests showed that these transcripts were responsive to both mycotoxigenic- and non-mycotoxigenic-associated Fusarium stress. In tests using the parents ‘CM82036’, ‘Remus’ and 14 double-haploid progeny that segregated for quantitative trait locus (QTL) Fhb1 on chromosome 3BS (syn. Qfhs.ndsu-3BS) (from ‘CM82036’ that confers DON tolerance), bZIP expression was significantly more DON-up-regulated in lines that inherited this QTL. Basal accumulation of the bZIP transcript in spikelets treated with Tween20 (control), DON and in DON-relative to Tween20-treated spikelets was negatively correlated with DON-induced bleaching above (but not below) the treated spikelets (AUDPCDON) (r = −0.41, −0.75 and −0.72, respectively; P ≤ 0.010). bZIP-specific PCR analysis of ‘Chinese spring’ and its 3BS deletion derivatives indicated that bZIP is located in chromosomal region(s) other than 3BS. These results, and the fact that a homologous cold-regulated wheat bZIP (wLIP19) maps to group 1 chromosomes suggests that wheat bZIP may participate in defence response cascades associated with Fhb1 and that there is a cross-talk between biotic and abiotic stress signalling pathways.



Basic leucine zipper protein

cv. or cvs



Differential display reverse transcriptase-polymerase chain reaction




Translation elongation factor 1 alpha


Fusarium head blight


Glyceraldehyde phosphate dehydrogenase


Genomic DNA


Long terminal repeat


Polymerase chain reaction




Quantitative trait loci


Reverse transcriptase-PCR


Structure-specific recognition protein



This research was funded by EU FP5 project FUCOMYR (QLRT-2000-02044) and Science Foundation Ireland. We thank Austrian and UK partners (Hermann Buerstmayr, IFA-Tulln, Austria and Paul Nicholson, JIC-UK), and the Wheat Genetics Resource Center of Kansas State University (Manhattan, KS, USA) for providing wheat seed. We thank Robert Proctor (USDA Agricultural Research Service, Peoria, IL, USA) for providing the Fusarium strains.


  1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acid Res 25:3389–3402PubMedCrossRefGoogle Scholar
  2. Andres MF, Melillo MT, Delibes A, Romero MD, Bleve-Zacheo T (2001) Changes in wheat root enzymes correlated with resistance to cereal cyst nematodes. New Phytol 152:243–354CrossRefGoogle Scholar
  3. Bai GH, Desjardins AE, Plattner RD (2002) Deoxynivalenol-nonproducing Fusarium graminearum causes initial infection, but does not cause disease spread in wheat spikes. Mycopathologia 153:91–98PubMedCrossRefGoogle Scholar
  4. Berberich T, Sano H, Kusano T (1999) Involvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maize. Mol Gen Genet 262:534–542PubMedCrossRefGoogle Scholar
  5. Berthiller F, Dall’Asta C, Schuhmacher R, Lemmens M, Adam G, Krska R (2005) Masked mycotoxins: determination of a deoxynivalenol glucoside in artificially and naturally contaminated wheat by liquid chromatography-tandem mass spectrometry. J Agric Food Chem 53:3421–3425PubMedCrossRefGoogle Scholar
  6. Boddu J, Cho S, Kruger WM, Muehlbauer GJ (2006) Transcriptome analysis of the barley-Fusarium graminearum interaction. Mol Plant Microbe Interact 19:407–417PubMedGoogle Scholar
  7. Brisson LF, Tenhaken R, Lamb CJ (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703–1712PubMedCrossRefGoogle Scholar
  8. Buerstmayr H, Steiner B, Hartl L, Griesser M, Angerer N, Lengauer D, Miedaner T, Schneider B, Lemmens M (2003) Molecular mapping of QTLs for Fusarium head blight resistance in spring wheat. II. Resistance to fungal penetration and spread. Theor Appl Genet 107:503–508PubMedCrossRefGoogle Scholar
  9. Bushnell WR, Seeland TM, Perkins-Veazie PM, Krueger DE, Collins JK, Russo VM (2004) The effects of deoxynivalenol on barley leaf tissues. In: Tsuyumu S, Leach JE, Shiraishi T, Wolpert T (eds) Genomic and genetic analysis of plant parasitism and defence. APS Press, St. Paul, pp 270–284Google Scholar
  10. Chang S, Puryer J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116Google Scholar
  11. Doohan FM, Weston G, Rezanoor HN, Parry DW, Nicholson P (1999) Development and use of a reverse transcriptionPCR assay to study expression of TRI5 by Fusarium species in vitro and in planta. Appl Environ Microbiol 65:3850–3854PubMedGoogle Scholar
  12. Doyle K (1996) DNA sequencing. In: Doyle K (ed) The sources for discovery, protocol and application guide. Promega corporation, USA, pp 147–162Google Scholar
  13. Doyle JJ, Doyle JL (1987) Isolation of DNA from fresh plant tissue. Focus 12:13–15Google Scholar
  14. Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295–307Google Scholar
  15. Grasser KD (2003) Chromatin-associated HMGA and HMGB proteins: versatile co-regulators of DNA-dependent processes. Plant Mol Biol 53:281–295PubMedCrossRefGoogle Scholar
  16. Grasser KD, Grill S, Duroux M, Launholt D, Thomsen MS, Nielsen BV, Nielsen HK, Merkle T (2004) HMGB6 from Arabidopsis thaliana specifies a novel type of plant chromosomal HMGB protein. Biochemistry 43:1309–1314PubMedCrossRefGoogle Scholar
  17. Han FP, Fedak G, Ouellet T, Dan H, Somers DJ (2005) Mapping of genes expressed in Fusarium graminearum-infected heads of wheat cultivar ‘Frontana’. Genome 48:88–96PubMedCrossRefGoogle Scholar
  18. Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42:462–468PubMedCrossRefGoogle Scholar
  19. Iiyama K, Lam TB-T, Stone BA (1994) Covalent cross-links in the cell wall. Plant Physiol 104:315–320PubMedGoogle Scholar
  20. Ivashuta S, Naumkina M, Gau M, Uchiyama K, Isobe S, Mizukami Y, Shimamoto Y (2002) Genotype-dependent transcriptional activation of novel repetitive elements during cold acclimation of alfalfa (Medicago sativa). Plant J 31:615–627PubMedCrossRefGoogle Scholar
  21. Jansen MAK, van den Noort RE, Tan MYA, Prinsen E, Lagrimini LM, Thorneley RNF (2001) Phenol-oxidizing peroxidases contribute to the protection of plants from ultraviolet radiation stress. Plant Physiol 126:1012–1023PubMedCrossRefGoogle Scholar
  22. Jones AM (2001) Programmed cell death in development and defence. Plant Physiol 125:94–97PubMedCrossRefGoogle Scholar
  23. Kang Z, Buchenauer H (1999) Immunocytochemical localization of Fusarium toxins in the wheat spikes infected by Fusarium culmorum. Physiol Mol Plant Pathol 55:275–288CrossRefGoogle Scholar
  24. Kang Z, Buchenauer H (2000) Cytology and ultra structure of the infection of wheat spikes by Fusarium culmorum. Mycol Res 104:1083–1093CrossRefGoogle Scholar
  25. Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33:102–106PubMedCrossRefGoogle Scholar
  26. Kong L, Anderson JM, Ohm HW (2005) Induction of wheat defense and stress-related genes in response to Fusarium graminearum. Genome 48:29–40PubMedCrossRefGoogle Scholar
  27. Kruger WM, Pritsch C, Chao S, Muehlbauer GJ (2002) Functional and comparative bioinformatic analysis of expressed genes from wheat spikes infected with Fusarium graminearum.Mol Plant Microbe Interact 15:445–455PubMedGoogle Scholar
  28. Lee SJ, Lee MY, Yi SY, Oh SK, Choi SH, Her NH, Choi D, Min BW, Yang SG, Harn CH (2002) PPI1: a novel pathogen-induced basic region-leucine zipper (bZIP) transcription factor from pepper. Mol Plant Microbe Interact 15:540–548PubMedGoogle Scholar
  29. Lee BJ, Park CJ, Kim SK, Kim KJ, Paek KH (2006) In vivo binding of hot pepper bZIP transcription factor CabZIP1 to the G-box region of pathogenesis-related protein 1 promoter. Biochem Biophys Res Commun 344:55–62PubMedCrossRefGoogle Scholar
  30. Lemmens M, Scholz U, Berthiller F, Dall’Asta C, Koutnik A, Schuhmacher R, Adam G, Buerstmayr H, Mesterházy Á, Krska R, Ruckenbauer P (2005) The ability to detoxify the mycotoxin deoxynivalenol co-localizes with a major QTL for Fusarium head blight resistance in wheat. Mol Plant Microbes Interact 18:1318–1324Google Scholar
  31. Liang P, Pardee AB (1992) Differential display of eukaryotic messenger RNA by means of polymerase chain reaction. Science 257:967–971PubMedCrossRefGoogle Scholar
  32. Liu SX, Anderson JA (2003) Marker assisted evaluation of Fusarium head blight resistant wheat germplasm. Crop Sci 43:760–766CrossRefGoogle Scholar
  33. Miller JD, Arnison PG (1986) Degradation of deoxynivalenol by suspension cultures of the Fusarium head blight resistant cultivar Frontana. Can J Plant Pathol 8:147–150CrossRefGoogle Scholar
  34. Parry DW, Jenkinson P, McLeod L (1995) Fusarium ear blight (scab) in small grains—a review. Plant Pathol 44:207–238Google Scholar
  35. Poppenberger B, Berthiller F, Lucyshyn D, Sieberer T, Schuhmacher R, Krska R, Kuchler K, Glössl J, Luschnig C, Adam G (2003) Detoxification of the Fusarium mycotoxin deoxynivalenol by a UDP-glucosyltransferase from Arabidopsis thaliana. J Biol Chem 278:47905–47914PubMedCrossRefGoogle Scholar
  36. Pritsch C, Muehbauer GJ, Bushnell WR, Somers DA, Vance CP (2000) Fungal development and induction of defense response gene during ear infection of wheat spikes by Fusarium graminearum. Mol Plant Microbe Interact 13:159–169PubMedGoogle Scholar
  37. Pritsch C, Vance CP, Bushnell WR, Somers DA, Hohn TM, Muehlbauer GJ (2001) Systemic expression of defense response genes in wheat spikes as a response to Fusarium graminearum infection. Physiol Mol Plant Pathol 58:1–12CrossRefGoogle Scholar
  38. Proctor RH, Hohn TM, McCormick SP (1995) Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol Plant Microbe Interact 8:593–601PubMedGoogle Scholar
  39. Sasaki K, Iwai T, Hiraga S, Kuroda K, Seo S, Mitsuhara I, Miyasaka A, Iwano M, Ito H, Matsui H, Ocashi Y (2004) Ten rice peroxidases redundantly respond to multiple stresses including infection with rice blast fungus. Plant Cell 6:1703–1712Google Scholar
  40. Schroeder HW, Christensen JJ (1963) Factors affecting the resistance of wheat to scab caused by Gibberella zeae. Phytopathology 53:831–838Google Scholar
  41. Shimizu H, Sato K, Berberich T, Miyazaki A, Ozaki R, Imai R, Kusano T (2005) LIP19, a basic region leucine zipper protein, is a Fos-like molecular switch in the cold signalling of rice plants. Plant Cell Physiol 46:1623–1634PubMedCrossRefGoogle Scholar
  42. Silar P, Picard M (1994) Increased longevity of EF-1 alpha high fidelity mutants in Podospora anserina. J Mol Biol 235:231–236PubMedCrossRefGoogle Scholar
  43. Yang SH, Berberich T, Sano H, Kusano T (2001) Specific association of transcripts of tbzF and tbz17, tobacco genes encoding basic region leucine zipper-type transcriptional activators, with guard cells of senescing leaves and/or flowers. Plant Physiol 127:23–32PubMedCrossRefGoogle Scholar
  44. Yang Z, Gilbert J, Fedak G, Somers DJ (2005) Genetic characterization of QTL associated with resistance to Fusarium head blight in a doubled-haploid spring wheat population. Genome 48:187–196PubMedGoogle Scholar
  45. Zhou W, Kolb FL, Riechers DE (2005) Identification of proteins induced or upregulated by Fusarium head blight infection in the spikes of hexaploid wheat (Triticum aestivum). Genome 48:770–780PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Khairul I. Ansari
    • 1
  • Stephanie Walter
    • 1
  • Josephine M. Brennan
    • 1
  • Marc Lemmens
    • 2
  • Sarah Kessans
    • 3
  • Angela McGahern
    • 1
  • Damian Egan
    • 1
  • Fiona M. Doohan
    • 1
  1. 1.Molecular Plant-Microbe Interactions Laboratory, School of Biology and Environmental Sciences, College of Life SciencesUniversity College DublinDublin 4Ireland
  2. 2.Institute for Plant Production Biotechnology, Department IFA-TullnBOKU, University of Natural Resources and Applied Life SciencesTullnAustria
  3. 3.Department of Botany and Plant Pathology, Lilly HallPurdue UniversityWest LafayetteUSA

Personalised recommendations