Skip to main content

Advertisement

Log in

Identification and differential induction of ABCG transporter genes in wheat cultivars challenged by a deoxynivalenol-producing Fusarium graminearum strain

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Fusarium head blight (FHB), predominantly caused by Fusarium graminearum, is a devastating disease that poses a serious threat to wheat (Triticum aestivum L.) production worldwide. A suppression subtractive hybridization cDNA library was constructed from F. graminearum infected spikes of a resistant Belgian winter wheat, Centenaire, exhibiting Type II resistance to FHB in order to identify differentially expressed members of full-size ABCG family. Members of the ABCG family are pleiotropic drug transporters allowing the movement of structurally unrelated metabolites, including pathogens-derived virulent compounds, across biological membranes and could be potentially involved in resistance to plant pathogens. In this study, five new full-size ABCG transporter expressed sequence tags TaABCG2, TaABCG3, TaABCG4, TaABCG5 and TaABCG6 have been identified. Time-course gene expression profiling between the FHB resistant Centenaire and the susceptible Robigus genotype showed that the newly isolated transcripts were differentially expressed up to 72 h-post inoculation. The respective genes encoding these transcripts were mapped to corresponding wheat chromosomes or chromosomal arms known to harbor quantitative trait loci for FHB resistance. Interestingly, these ABCG transcripts were also induced by deoxynivalenol (DON) treatment of germinating wheat seeds and the toxin treatment inhibited root and hypocotyl growth. However, the hypocotyl of the FHB resistant cultivar Centenaire was less affected than that of the susceptible cultivar Robigus, reflecting more likely the genotype-dependent differential expression pattern of the identified ABCG genes. This work emphasizes the potential involvement of ABCG transporters in wheat resistance to FHB, at least in part through the detoxification of the pathogen-produced DON.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Kazan K, Gardiner D, Manners J (2011) On the trail of a cereal killer: recent advances in Fusarium graminearum pathogenomics and host resistance. Mol Plant Pathol 13:399–413

    Article  PubMed  Google Scholar 

  2. Bai G, Shaner G (2004) Management and resistance in wheat and barley to Fusarium head blight. Ann Rev Phytopathol 42:135–161

    Article  CAS  Google Scholar 

  3. Foroud N, Eudes F (2009) Trichothecenes in cereal grains. Int J Mol Sci 10:147–173

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Walter S, Nicholson P, Doohan F (2010) Action and reaction of host and pathogen during Fusarium head blight disease. New Phytol 185:54–66

    Article  CAS  PubMed  Google Scholar 

  5. Jansen C, Von Wettstein D, Schafer W, Kogel K, Felk A, Maier F (2005) Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc Nat Acad Sci 102:16892–16897

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Rocha O, Ansari K, Doohan F (2005) Effects of trichothecene mycotoxins on eukaryotic cells: a review. Food Addit Contam 22:369–378

    Article  CAS  PubMed  Google Scholar 

  7. Masuda D, Ishida M, Yamaguchi K, Yamaguchi I, Kimura M, Nishiuchi T (2007) Phytotoxic effects of trichotechenes on the growth and morphology of Arabidopsis thaliana. J Exp Bot 58:1617–1626

    Article  CAS  PubMed  Google Scholar 

  8. Desmond O, Manners J, Stephens A, Maclean D, Schenk P, Gardiner D, Munn A, Kazan K (2008) The Fusarium mycotoxins deoxynivalenol elicits hydrogen peroxide production, programmed cell death and defense responses in wheat. Mol Plant Pathol 9:435–445

    Article  CAS  PubMed  Google Scholar 

  9. Li G, Yen Y (2008) Jasmonate and ethylene signaling pathway may mediate Fusarium head blight resistance in wheat. Crop Sci 48:1888–1896

    Article  Google Scholar 

  10. Brown NA, Urban M, Van de Meene A, Hammond-Kosack K (2010) The infection biology of Fusarium graminearum: defining the pathways of spikelet to spikelet colonization in wheat ears. Fungal Biol 114:555–571

    Article  PubMed  Google Scholar 

  11. Jia H, Cho S, Muehlbauer G (2009) Transcriptome analysis of a wheat near-isogenic line pair carrying Fusarium head blight-resistant and -susceptible alleles. Mol Plant Microbe Int 22:1366–1378

    Article  CAS  Google Scholar 

  12. Buerstmayr H, Ban T, Anderson A (2009) QTL mapping and marker-assisted selection for Fusarium head blight resistance in wheat: a review. Plant Breed 128:1–26

    Article  CAS  Google Scholar 

  13. Schroeder HW, Christensen JJ (1963) Factors affecting resistance of wheat to scab caused by Gibberella zeae. Phytopathology 53:831–838

    Google Scholar 

  14. Mesterhazy A (1995) Types and components of resistance to Fusarium head blight of wheat. Plant Breed 114:377–386

    Article  Google Scholar 

  15. Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Bio Rep 9:208–218

    Article  CAS  Google Scholar 

  16. Kruger W, Pritsch C, Chao S, Muehlbauer G (2002) Functional and comparative bioinformatic analysis of expressed genes from wheat spikes infected with Fusarium graminearum. Mol Plant Microbe Int 15:445–455

    Article  CAS  Google Scholar 

  17. Kong L, Ohm H, Anderson JM (2007) Expression analysis of defense- related genes in wheat in response to infection by Fusarium graminearum. Genome 50:1038–1048

    Article  CAS  PubMed  Google Scholar 

  18. Walter S, Brennan J, Arunachalam C, Ansari K, Hu X, Khan M, Trognitz F, Trognitz B, Leonard G, Egan D, Doohan F (2008) Components of the gene network associated with genotype- dependent response of wheat to the Fusarium mycotoxins deoxynivalenol. Func Integr Genomics 8:421–427

    Article  CAS  Google Scholar 

  19. Golkari S, Gilbert J, Prashar S, Procunier JD (2007) Microarray analysis of Fusarium graminearum-induced wheat genes: identification of organ-specific and differentially expressed genes. Plant Biotechnol J 5:38–49

    Article  CAS  PubMed  Google Scholar 

  20. Golkari S, Gilbert J, Ban T, Procunier JD (2009) QTL- specific microarray gene expression analysis of wheat resistance to Fusarium head blight in Sumai-3 and two susceptible NILs. Genome 52:409–418

    Article  CAS  PubMed  Google Scholar 

  21. Lulin M, Yi S, Aizhong C, Zengjun Q, Liping X, Peidu C, Dajun L, Xiue W (2010) Molecular cloning and characterization of an up-regulated UDP-glucosyltransferase gene induced by DON from Triticum aestivum L. cv Wangshuibai. Mol Biol Rep 37:785–795

    Article  PubMed  Google Scholar 

  22. Lucyshyn D, Busch B, Abolmaali S, Steiner B, Chandler E, Sanjarian F, Mousavi A, Nicholson P, Buerstmayr H, Adam G (2007) Cloning and characterization of ribosomal protein L3 (RPL3) gene family from Triticum aestivum. Mol Genet Genomics 277:507–517

    Article  CAS  PubMed  Google Scholar 

  23. Schweiger W, Boddu J, Shin S, Poppenberger B, Berthiller F, Lemmens M, Muehlbauer G, Adam G (2010) Validation of a candidate deoxynivalenol-inactivating UDP-glycosyltransferase from barley by heterologous expression in yeast. Mol Plant Microbe Int 23:977–986

    Article  CAS  Google Scholar 

  24. Balzi E, Wang M, Leterme S, Van Dyck L, Goffeau A (1994) PDR5, a novel yeast multidrug resistance conferring transporter controlled by the transcriptional regulator PDR1. J Biol Chem 269:2206–2214

    CAS  PubMed  Google Scholar 

  25. Muhitch MJ, McCormick SP, Alexander NJ, Hohn TM (2000) Transgenic expression of the TRI101 or PDR5 gene increase resistance of tobacco to the phytotoxic effect of the trichothecenes 4, 15-diacetoxyscirpenol. Plant Sci 157:201–207

    Article  CAS  PubMed  Google Scholar 

  26. Mitterbauer R, Adam G (2002) Saccharomyces cerevisiae and Arabidopsis thaliana: useful model systems for the identification of molecular mechanisms involved in resistance of plants to toxins. Eur J Plant Pathol 108:699–703

    Article  CAS  Google Scholar 

  27. Rea PA (2007) Plant ATP-binding cassette transporters. Ann Rev Plant Biol 58:347–375

    Article  CAS  Google Scholar 

  28. Jasinski M, Banasiak J, Radom M, Kalitkewicz A, Figlerowicz M (2009) Full-size ABC transporters from the ABCG subfamily in Medicago truncatula. Mol Plant Microbe Int 22:921–931

    Article  CAS  Google Scholar 

  29. Verrier PJ, Bird D, Burla B et al (2008) Plant ABC proteins- a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159

    Article  CAS  PubMed  Google Scholar 

  30. Crouzet J, Trombik T, Fraysse AS, Boutry M (2006) Organization and function of the plant pleiotropic drug resistance ABC transporter family. FEBS Lett 580:1123–1130

    Article  CAS  PubMed  Google Scholar 

  31. Lamping E, Baret P, Holmes A, Monk B, Goffeau A, Cannon R (2010) Fungal PDR transporters: phylogeny, topology, motifs and function. Fungal Genet Biol 47:127–142

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Moons A (2008) Transcriptional profiling of the PDR gene family in rice roots in response to plant growth regulators, redox perturbations and weak acid organic stresses. Planta 229:53–71

    Article  CAS  PubMed  Google Scholar 

  33. Ruocco M, Ambrosino P, Lanzuise S, Woo S, Lorito M, Scala F (2011) Four potato (Solanum tuberosum) ABCG transporters and their expression in response to abiotic factors and Phytophthora infestans infection. J Plant Physiol 168:2225–2233

    Article  CAS  PubMed  Google Scholar 

  34. Migocka M, Papierniak A, Warzybok A, Klobus G (2012) CsPDR8 and CsPDR12, two of the 16 pleiotropic drug resistance genes in cucumber, are transcriptionally regulated by phytohormones and auxin herbicide in roots. Plant Growth Regul 67:171–184

    Article  CAS  Google Scholar 

  35. Zhang L, Lu X, Shen Q et al (2012) Identification of putative Artemisia annua ABCG transporter unigenes related to artemisinin yield following expression analysis in different plant tissues and is response to methyl jasmonate and abscisic acid treatment. Plant Mol Biol Rep 30:838–847

    Article  CAS  Google Scholar 

  36. Stukkens Y, Bultreys A, Grec S, Trombik T, Vanham D, Boutry M (2005) NpPDR1, a pleiotropic drug resistance-type ATP-binding cassette transporter from Nicotiana plumbaginifolia, plays a major role in plant pathogen defense. Plant Physiol 139:341–352

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Bultreys A, Trombik T, Drozak A, Boutry (2009) Nicotiana plumbaginifolia plants silenced for the ATP-binding cassette transporter gene NpPDR1 show increased susceptibility to a group of fungal and oomycete pathogens. Mol Plant Pathol 10:651–663

    Article  CAS  PubMed  Google Scholar 

  38. Jasinski M, Stukkens Y, Degand H, Purnelle B, Marchand-Brynaert J, Boutry M (2001) A plant plasma membrane ATP binding cassette-transporter is involved in antifungal terpenoid secretion. Plat Cell 13:1095–1107

    Article  CAS  Google Scholar 

  39. Sasabe M, Toyoda K, Shirashi T, Inagaki Y, Ichinose Y (2002) cDNA cloning and characterization of tobacco ABC transporter: NtPDR1 is a novel elicitor-responsive gene. FEBS Lett 518:164–168

    Article  CAS  PubMed  Google Scholar 

  40. Campbell EJ, Schenk PM, Kazan K, Penninckx IA, Anderson JP, Maclean DJ, Cammue B, Ebert P, Manners J (2003) Pathogen-responsive expression of a putative ATP-binding cassette transporter gene conferring resistance to the diterpenoid sclareol is regulated by multiple defense signaling pathways in Arabidopsis. Plant Physiol 133:1272–1284

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. Eichhorn H, Klinghammer M, Becht P, Tenhaken R (2006) Isolation of a novel ABC-transporter gene from soybean induced by salicylic acid. J Exp Bot 57:2193–2201

    Article  CAS  PubMed  Google Scholar 

  42. Stein M, Dittgen J, Sanchez-Rodriguez C, Hou B, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to non-host resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731–746

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Kang Z, Buchenauer H (1999) Immunocytochemical localization of Fusarium toxins in infected wheat spikes by Fusarium culmorum. Physiol Mol Plant Pathol 55:275–288

    Article  CAS  Google Scholar 

  44. Smart CC, Fleming AJ (1996) Hormonal and environmental regulation of plant PDR5-like ABC transporter. J Biol Chem 271:19351–19357

    Article  CAS  PubMed  Google Scholar 

  45. Ducos E, Fraysse A, Boutry M (2005) NtPDR3, an iron-deficiency inducible ABC transporter in Nicotiana tabacum. FEBS Lett 579:6791–6795

    Article  CAS  PubMed  Google Scholar 

  46. Lee M, Lee K, Lee J, Noh EW, Lee Y (2005) AtPDR12 contributes to lead resistance in Arabidopsis. Plant Physiol 138:827–836

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Kim DY, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 50:207–218

    Article  CAS  PubMed  Google Scholar 

  48. Krattinger S, Lagudah E, Spielmeyer W, Singh R, Hueta-Espino J, McFadden H, Bossolini E, Selter L, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363

    Article  CAS  PubMed  Google Scholar 

  49. Shang Y, Xiao J, Ma LL, Wang HY, Qi ZJ, Chen PD (2009) Characterization of a PDR type transporter gene from wheat (Triticum aestivum L.). Chin Sci Bull 54:3249–3257

    Article  CAS  Google Scholar 

  50. Chen G, Komatsuda T, Feng J, Nawrathd C et al (2011) An ATP-binding cassette subfamily G full transporter is essential for the retention of leaf water in both wild barley and rice. Proc Nat Acad Sci 108:12354–12359

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  51. Duvick JP, Rood T, Rao AG, Marshak DR (1992) Purification and characterization of a novel antimicrobial peptide from maize (Zea mays L.) kernels. J Biol Chem 267:18814–18820

    CAS  PubMed  Google Scholar 

  52. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  53. Prasad M, Varshney RK, Roy JK, Balyan HS, Gupta PK (2000) The use of microsatellite for detecting DNA polymorphism genotype identification and genetic diversity in wheat. Theor Appl Genet 100:584–592

    CAS  Google Scholar 

  54. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. New Age International Pvt Ltd, New Delhi

    Google Scholar 

  55. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  56. Diatchenko L, Chris L, Campbell A, Chenchi A, Moqadam F, Huang B, Lukyanov K, Gurskaya N, Sverdlov E, Siebert P (1996) Suppression subtractive hybridization: a method for generation differentially regulated or tissue-specific cDNA probes and libraries. Proc Nat Acad Sci 93:6025–6039

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  57. Kang J, Park J, Choi H, Burla B, Kretzschmar T, Lee Y, Martinoia E (2011) Plant ABC transporters. Arabidopsis B 2011(9):e0153. doi:10.1199/tab.0153

    Article  Google Scholar 

  58. Boutigny AL, Richard-Forget F, Barreau C (2008) Natural mechanisms for cereal resistance to the accumulation of Fusarium trichothecenes. Eur J Plant Pathol 121:411–423

    Article  CAS  Google Scholar 

  59. Poppenberger B, Berthiller F, Lucyshyn D, Sieberer T, Schuhmacher R, Krska R, Kuchler K, Glossl J, Luschnig C, Adam G (2003) Detoxification of the Fusarium mycotoxins deoxynivalenol by a UDP- glucosyltransferase from Arabidopsis thaliana. J Biol Chem 278:47905–47914

    Article  CAS  PubMed  Google Scholar 

  60. Moons A (2003) Ospdr9, which encodes a PDR-type ABC transporter, is induced by heavy metals, hypoxic stress and redox perturbations in rice roots. FEBS Lett 553:370–376

    Article  CAS  PubMed  Google Scholar 

  61. Van den Brule S, Smart CC (2002) The plant PDR family of ABC transporters. Planta 216:95–106

    Article  PubMed  Google Scholar 

  62. Bienert MD, Siegmund SEG, Drozak A, Trombik T, Bultreys A, Baldwin IT, Boutry M (2012) A pleiotropic drug resistance transporter in Nicotiana tabacum is involved in defense against the herbivore Manduca sexta. Plant J 72:745–757

    Article  CAS  PubMed  Google Scholar 

  63. Liu S, Hall MD, Griffey C, McKendry AL (2009) Meta-analysis of QTL associated with Fusarium head blight resistance in wheat. Crop Sci 49:1955–1968

    Article  CAS  Google Scholar 

  64. Zwart R, Muyelle H, Van Bockstaele E, Roldan-Ruiz I (2008) Evaluation of genetic diversity of Fusarium head blight resistance in European winter wheat. Theor Appl Genet 117:813–828

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yordan Muhovski.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 267 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Muhovski, Y., Jacquemin, JM. & Batoko, H. Identification and differential induction of ABCG transporter genes in wheat cultivars challenged by a deoxynivalenol-producing Fusarium graminearum strain. Mol Biol Rep 41, 6181–6194 (2014). https://doi.org/10.1007/s11033-014-3497-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-014-3497-7

Keywords

Navigation