Plant Molecular Biology

, Volume 64, Issue 3, pp 305–318 | Cite as

Transcriptional regulation of genes involved in the pathways of biosynthesis and supply of methyl units in response to powdery mildew attack and abiotic stresses in wheat

  • Nazmul H. Bhuiyan
  • Weiping Liu
  • Guosheng Liu
  • Gopalan Selvaraj
  • Yangdou Wei
  • John King


From a library of 3,000 expression sequence tags (ESTs), derived from the epidermis of a diploid wheat (Triticum monococcum) inoculated with Blumeria graminis f. sp. tritici (Bgt), we cloned 23 cDNAs representing 12 genes that are involved in the pathways of biosynthesis and supply of methyl units. We studied the transcription of these genes to investigate how the methyl units are generated and regulated in response to Bgt infection and abiotic stresses in wheat. Expression of 5, 10-methylene-tetrahydrofolate reductase, methionine synthase, S-adenosylmethionine synthetase, and S-adenosylhomocystein hydrolase transcripts were highly induced at an early stage of infection. This induction was specific to the epidermis and linked to host cell wall apposition (CWA) formation, suggesting that the pathways for generation of methyl units are transcriptionally activated for the host defense response. Levels of S-adenosylmethionine decarboxylase, caffeic acid 3-O-methyltransferase, 1-aminocyclopropane-1-carboxylate oxidase mRNA, but not phosphoethanolamine N-methyltransferase and nicotianamine synthase mRNA, were up-regulated after infection and showed similar expression patterns to genes involved in the pathways of generation of methyl units, revealing possible routes of methyl transfer towards polyamine, lignin and ethylene biosynthesis rather than glycine betaine and nicotianamine in response to Bgt attack. After imposing various abiotic stresses, genes involved in the pathways of generation and supply of methyl units were also up-regulated differentially, suggesting that the generation of sufficient methyl units at an early stage might be crucial to the mitigation of multiple stresses.


C1 metabolism Gene expression pattern Stress resistance Transmethylation 



5, 10-Methylene-tetrahydrofolate dehydrogenase/5, 10-methenyl-tetrahydrofolate cyclohydrolase


5, 10-Methylene-tetrahydrofolate reductase


Cobalamin-independent methionine synthase


S-adenosylmethionine synthetase


S-adenosylhomocystein hydrolase


Serine hydroxy methyltransferase


S-adenosyl methionine decarboxylase


Caffeic acid 3-O-methyltransferase


1-Aminocyclopropane-1-carboxylate oxidase


Phosphoethanolamine N-methyltransferase


Nicotianamine synthase




Primary germ tube


Appressorial germ tube


Pathogenesis related


3, 3′-Diaminobenzidine


Cell wall apposition



This work was supported by the Natural Sciences and Engineering Research Council of Canada in the form of a Discovery Grant to JK. We thank R. Hirji for technical assistance, and the DNA technology unit of NRC-PBI Saskatoon for sequencing and oligonucleotide synthesis.


  1. Aist JR, Israel HW (1977) Papilla formation: timing and significance during penetration of barley coleoptiles by Erysiphe graminis hordei. Phytopathology 67:455–461Google Scholar
  2. Bushnell WR (2002) The role of powdery mildew research in understanding host-parasite interaction: past, present, and future. In: Belanger RR, Bushnell WR (eds) The powdery mildew: a comprehensive treatise. APS Press, St. Paul, MN, pp 1–12Google Scholar
  3. Campbell M, Sederoff RR (1996) Variation in lignin content and composition. Plant Physiol 110:3–13PubMedGoogle Scholar
  4. Chen N, Goodwin PH, Hsiang T (2003) The role of ethylene during the infection of Nicotiana tabacum by Colletotrichum destructivum. J Exp Bot 54:2449–2456PubMedCrossRefGoogle Scholar
  5. Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661–677PubMedCrossRefGoogle Scholar
  6. Collinge DB, Gregersen PL, Thordal-Christensen H (2002) The nature and role of defense response genes in cereals. In: Belanger RR, Bushnell WR (eds) The powdery mildew: a comprehensive treatise. APS Press, St. Paul, MN, pp 146–160Google Scholar
  7. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu J-L, Hückelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–977PubMedCrossRefGoogle Scholar
  8. Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11:80–88PubMedCrossRefGoogle Scholar
  9. Cowley T, Walters DR (2002) Polyamine metabolism in barley reacting hypersensitively to the powdery mildew fungus Blumeria graminis f. sp. hordei. Plant Cell Environ 25:461–468CrossRefGoogle Scholar
  10. Espartero J, Pintor-Toro JA, Pardo JM (1994) Differential accumulation of S-adenosyl methionine synthetase transcripts in response to salt stress. Plant Mol Biol 25:217–227PubMedCrossRefGoogle Scholar
  11. Gowri G, Bugos RC, Campbell WH, Maxwell CA, Dixon RA (1991) Stress responses in alfalfa (Medicago sativa L.). X. Molecular cloning and expression of S-adenosyl-L-methionine: caffeic acid 3-O-methyltransferase, a key enzyme of lignin biosynthesis. Plant Physiol 97:7–14PubMedGoogle Scholar
  12. Greenshields DL, Liu G, Selvaraj G, Wei Y (2005) Differential regulation of wheat quinine reductases in response to powdery mildew infection. Planta 222:867–875PubMedCrossRefGoogle Scholar
  13. Hanson AD, Roje S (2001) One carbon metabolism in higher plants. Annu Rev Plant Physiol Plant Mol Biol 52:119–137PubMedCrossRefGoogle Scholar
  14. Higuchi T (1981) Biosynthesis of lignin. In: Tanner W, Loewus FA (eds) Plant carbohydrates II. Encyclopedia of plant physiology, NS, vol 13B. Springer, Berlin, pp 194–224Google Scholar
  15. Hückelhoven R, Kogel K-H (2003) Reactive oxygen intermediates in plant-microbe interactions: who is who in powdery mildew resistance? Planta 216:891–902PubMedGoogle Scholar
  16. Hückelhoven R, Fodor J, Preis C, Kogel K-H (1999) Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation. Plant Physiol 119:1251–1260CrossRefPubMedGoogle Scholar
  17. Kawalleck P, Plesch G, Hahlbrock K, Somssich IE (1992) Induction by fungal elicitor of S-adenosyl-L-methionine synthetase and S-adenosyl-L-homocysteine hydrolase mRNAs in cultured cells and leaves of Petroselinum crispum. Proc Natl Acad Sci USA 89:4713–4717PubMedCrossRefGoogle Scholar
  18. Lewis NG, Yamamoto E (1990) Lignin: occurrence, biogenesis and biodegradation. Annul Rev Plant Physiol Plant Mol Biol 41:455–496CrossRefGoogle Scholar
  19. Li R, Moore M, King J (2003) Investigating the regulation of one-carbon metabolism in Arabidopsis thaliana. Plant Cell Physiol 44:233–241PubMedCrossRefGoogle Scholar
  20. Liu G, Sheng X, Greenshields DL, Ogieglo A, Kaminskyj S, Selvaraj G, Wei Y (2005) Profiling of wheat class III peroxidase genes derived from powdery mildew-attacked epidermis reveals distinct sequence-associated expression patterns. Mol Plant Micro Interac 18:730–741CrossRefGoogle Scholar
  21. McNeil SD, Nuccio ML, Ziemak MJ, Hanson AD (2001) Enhanced synthesis of choline and glycine betaine in transgenic tobacco plants that overexpress phosphoethanolamine N-methyltransferase. Proc Natl Acad Sci USA 98:10001–10005PubMedCrossRefGoogle Scholar
  22. Mellersh DG, Foulds IV, Higgins VJ, Heath MC (2002) H2O2 plays different roles in determining penetration failure in three diverse plant–fungal interactions. Plant J 29:257–268PubMedCrossRefGoogle Scholar
  23. Moffatt BA, Weretilnyk EA (2001) Sustaining S-adenosylmethionine-dependent methyltransferase activity in plant cells. Physiol Plantarum 113:435–442CrossRefGoogle Scholar
  24. Moreno JI, Martín R, Castresana C (2004) Arabidopsis SHMT1, a serine hydroxymethyltransferase that functions in the photorespiratory pathway influences resistance to biotic and abiotic stress. Plant J 41:451–463CrossRefGoogle Scholar
  25. Peleman J, Boerjan W, Engler G, Seurinck J, Botterman J, Alliotte T, Van Montagu M, Inzé D (1989) Strong cellular preference in the expression of a housekeeping gene of Arabidopsis thaliana encoding S-adenosylmethionine synthetase. Plant Cell 1:81–93PubMedCrossRefGoogle Scholar
  26. Prabhu V, Chatson KB, Abrams GD, King J (1996) 13C nuclear magnetic resonance detection of interactions of serine hydroxymethyltransferase with C1-tetrahydrofolate synthase and glycine decarboxylase complex activities in Arabidopsis. Plant Physiol 112:207–216PubMedCrossRefGoogle Scholar
  27. Ride JP, Barber MS (1987) The effects of various treatments on induced lignification and the resistance of wheat to fungi. Physiol Mol Plant Pathol 31:349–360CrossRefGoogle Scholar
  28. Scheideler M, Schlaich NL, Fellenberg K, Beissbarth T, Hauser NC, Vingron M, Slusarenko AJ, Hoheisel JD (2002) Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays. J Biol Chem 277:10555–10561PubMedCrossRefGoogle Scholar
  29. Schröder G, Eichel J, Breinig S, Schröder J (1997) Three differentially expressed S-adenosylmethionine synthetases from Catharanthus roseus: molecular and functional characterization. Plant Mol Biol 33:211–222PubMedCrossRefGoogle Scholar
  30. Tabor CW, Tabor H (1984) Methionine adenosyltransferase (S-adenosylmethionine synthetase) and S-adenosylmethionine decarboxylase. Adv Enzymol 56:251–282PubMedGoogle Scholar
  31. Tabuchi T, Kawaguchi Y, Azuma T, Nanmori T, Yasuda T (2005) Similar regulation patterns of choline Monooxygenase, phosphoethanolamine N-methyltransferase and S-adenosyl-L-methionine synthetase in leaves of the halophyte Atriplex nummularia L. Plant Cell Physiol 46:505–513PubMedCrossRefGoogle Scholar
  32. Thordal-Christensen H, Zhang Z, Wei YD, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194CrossRefGoogle Scholar
  33. Trujillo M, Kogel K-H, Hückelhoven R (2004) Superoxide and hydrogen peroxide play different roles in the nonhost interaction of barley and wheat with inappropriate formae speciales of Blumeria graminis. Mol Plant Microbe Interact 17:304–312PubMedCrossRefGoogle Scholar
  34. Von Röpenack E, Parr A, Schulze-Lefert P (1998) Structural analysis and dynamics of soluble and cell wall-bound phenolics in a broad-spectrum resistance to the powdery mildew fungus in barley. J Biol Chem 273:9013–9022CrossRefGoogle Scholar
  35. Waditee R, Bhuiyan NH, Rai V, Aoki K, Tanaka Y, Hibino T, Suzuki S, Takano J, Jagendorf AT, Takabe T, Takabe T (2005) Genes for direct methylation of glycine provide high levels of glycine betaine and abiotic-stress tolerance in Synechococcus and Arabidopsis. Proc Natl Acad Sci USA 102:1318–1323PubMedCrossRefGoogle Scholar
  36. Wei YD, Zhang Z, Anderson CH, Schmelzer E, Gregersen PL, Collinge DB, Smedegaard-Petersen V, Thordal-Christensen H (1998) An epidermis/papilla-specific oxalate oxidase-like protein in the defense response of barley attacked by the powdery mildew fungus. Plant Mol Biol 36:101–112PubMedCrossRefGoogle Scholar
  37. Zeyen RJ, Carver TLW, Lyngkjaer MF (2002) Epidermal cell papillae. In: Belanger RR, Bushnell WR (eds) The powdery mildew: a comprehensive treatise. APS Press, St. Paul, MN, pp 107–125Google Scholar
  38. Zierold U, Scholz U, Schweizer P (2005) Transcriptome analysis of mlo-mediated resistance in the epidermis of barley. Mol Plant Pathol 6:139–151CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Nazmul H. Bhuiyan
    • 1
  • Weiping Liu
    • 1
  • Guosheng Liu
    • 1
  • Gopalan Selvaraj
    • 2
  • Yangdou Wei
    • 1
  • John King
    • 1
  1. 1.Department of BiologyUniversity of SaskatchewanSaskatoonCanada
  2. 2.Plant Biotechnology InstituteNational Research Council of CanadaSaskatoonCanada

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