Skip to main content

Advertisement

Log in

Characterization of a novel wheat NAC transcription factor gene involved in defense response against stripe rust pathogen infection and abiotic stresses

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Proteins encoded by the NAC gene family constitute one of the largest plant-specific transcription factors, which have been identified to play many important roles in both abiotic and biotic stress adaptation, as well as in plant development regulation. In the current paper, a full-length cDNA sequence of a novel wheat NAC gene, designated as TaNAC4, was isolated using in silico cloning and the reverse transcription PCR (RT–PCR) methods. TaNAC4 sharing high homology with rice OsNAC4 gene was predicted to encode a protein of 308 amino acid residues, which contained a plant-specific NAC domain in the N-terminus. Transient expression analysis indicated that the deduced TaNAC4 protein was localized in the nucleus of onion epidemical cells. Yeast one-hybrid assay revealed that the C-terminal region of the TaNAC4 protein had transcriptional activity. The expression of TaNAC4 was largely higher in the wheat seedling roots, than that in leaves and stems. TaNAC4 transcript in wheat leaves was induced by the infection of strip rust pathogen, and also by exogenous applied methyl jasmonate (MeJA), ABA and ethylene. However, salicylic acid (SA) had no obvious effect on TaNAC4 expression. Environmental stimuli, including high salinity, wounding, and low-temperature also induced TaNAC4 expression. These results indicate that this novel TaNAC4 gene functions as a transcriptional activator involved in wheat response to biotic and abiotic stresses.

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

Similar content being viewed by others

Abbreviations

NAC:

NAM ATAF1/2 CUC2

PST :

Puccinia striiformis f. sp. tritici Westend

RT-PCR:

Reverse transcription polymerase chain reaction

qRT-PCR:

Quantitative reverse transcription polymerase chain reaction

MeJA:

Methyl jasmonate

ET:

Ethylene

ABA:

Abscisc acid

SA:

Salicylic acid

Fp:

Forward primer

Rp:

Reverse primer

Hpi:

Hour post inoculation

Hpt:

Hour post treatment

BLAST:

Basic local alignment search tool

ORF:

Open reading frame

GFP:

Green fluorescent protein

HR:

Hypersensitive response

X-GAL:

β-d-Galactopyranoside

CaMV:

Cauliflower mosaic virus

VIGS:

Virus induced gene silencing

RNAi:

RNA interference

References

  1. Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403. doi:10.1146/annurev.arplant.47.1.377

    Article  CAS  PubMed  Google Scholar 

  2. Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross-tolerance to stress. The central role of “redox” and abscisic acid-mediated controls. Plant Physiol 129:460–468. doi:10.1104/pp.011021

    Article  CAS  PubMed  Google Scholar 

  3. Huang J, Wang J, Zhang H (2005) Rice ZFP15 gene encoding for a novel C2H2-type zinc finger protein lacking DLN box, is regulated by spike development but not by abiotic stresses. Mol Biol Rep 32(3):177–183. doi:10.1007/s11033-005-2338-0

    Article  CAS  PubMed  Google Scholar 

  4. Nakashima K, Yamaguchi-Shinozaki K (2006) Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol Plant 126:62–71. doi:10.1111/j.1399-3054.2005.00592.x

    Article  CAS  Google Scholar 

  5. Umezawa T, Fujita M, Fujita Y, Yamaquchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17:113–122. doi:10.1016/j.copbio.2006.02.002

    CAS  PubMed  Google Scholar 

  6. Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress responsive promoters. Trends Plant Sci 10:88–94. doi:10.1016/j.tplants.2004.12.012

    Article  CAS  PubMed  Google Scholar 

  7. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803. doi:10.1146/annurev.arplant.57.032905.105444

    Article  CAS  PubMed  Google Scholar 

  8. Agarwal P, Agarwal PK, Joshi AJ, Sopory SK, Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abiotic stress tolerance and activates downstream stress-responsive genes. Mol Biol Rep 37(2):1125–1135. doi:10.1007/s11033-009-9885-8

    Article  CAS  PubMed  Google Scholar 

  9. Chen WQ, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA, Budworth PR, Tao Y, Xie Z, Chen X, Lam S, Kreps JA, Harper JF, Si-Ammour A, Mauch-Mani B, Heinlein M, Kobayashi K, Hohn T, Dangl JL, Wang X, Zhu T (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574

    Article  CAS  PubMed  Google Scholar 

  10. Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ 27:521–549. doi:10.1111/j.1365-3040.2003.01158.x

    Article  CAS  Google Scholar 

  11. Lin JF, Wu SH (2004) Molecular events in senescing Arabidopsis leaves. Plant J 39:612–628. doi:10.1111/j.1365-313X.2004.02160.x

    Article  CAS  PubMed  Google Scholar 

  12. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver C (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signaling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585. doi:10.1111/j.1365-313X.2005.02399.x

    Article  CAS  PubMed  Google Scholar 

  13. Yang Y, Wu J, Zhu K, Liu L, Chen F, Yu D (2009) Identification and characterization of two chrysanthemum (Dendronthema × moriforlium) DREB genes, belonging to the AP2/EREBP family. Mol Biol Rep 36(1):71–81. doi:10.1007/s11033-007-9153-8

    Article  CAS  PubMed  Google Scholar 

  14. Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87. doi:10.1016/j.tplants.2004.12.010

    Article  CAS  PubMed  Google Scholar 

  15. Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis, analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857

    Article  CAS  PubMed  Google Scholar 

  16. Duval M, Hsieh T-F, Kim SY, Thomas TL (2002) Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. Plant Mol Biol 50:237–248. doi:10.1023/A:1016028530943

    Article  CAS  PubMed  Google Scholar 

  17. Ren T, Qu F, Morris TJ (2000) HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. Plant Cell 12:1917–1926

    Article  CAS  PubMed  Google Scholar 

  18. Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036. doi:10.1101/gad.852200

    Article  CAS  PubMed  Google Scholar 

  19. Gong W, Shen YP, Ma LG, Pan L, Du YL, Wang DH, Yang JY, Hu LD, Liu XF, Dong CX, Ma X, Chen YH, Yang XY, Gao Y, Zhu D, Tan X, Mu JY, Zhang DB, Liu YL, Dinesh-Kumar SP, Li Y, Wang XP, Gu HY, Qu LJ, Bai SN, Lu YT, Li JY, Zhao JD, Zuo J, Huang H, Deng XW, Zhu YX (2004) Genome-wide ORFeome cloning and analysis of Arabidopsis transcription factor genes. Plant Physiol 135(2):773–782. doi:10.1104/pp.104.042176

    Article  CAS  PubMed  Google Scholar 

  20. Xiong YQ, Liu TY, Tian CG, Sun SH, Li JY, Chen MS (2005) Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 59(1):191–203. doi:10.1007/s11103-005-6503-6

    Article  CAS  PubMed  Google Scholar 

  21. Souer E, Kloos D, Mol J, Koes R, Vanhouwelingen A (1996) The No Apical Meristem gene of petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordial boundaries. Cell 85:159–170. doi:10.1016/S0960-9822(95)00282-X

    Article  CAS  PubMed  Google Scholar 

  22. Takada S, Hibara K, Ishida T, Tasaka M (2001) The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128:1127–1135

    CAS  PubMed  Google Scholar 

  23. Vroemen CW, Mordhorst AP, Albrecht C, Kwaaitaal MACJ, de Vries S (2003) The CUP-SHAPED COTYLEDON1 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15:1563–1577

    Article  CAS  PubMed  Google Scholar 

  24. Sablowski RW, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103

    Article  CAS  PubMed  Google Scholar 

  25. Collinge M, Boller T (2001) Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Mol Biol 46(5):521–529. doi:10.1023/A:1010639225091

    Article  CAS  PubMed  Google Scholar 

  26. Hegedus D, Yu M, Baldwin D, Margaret G, Sharpe A, Parkin I, Whitwill S, Lydiate D (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Mol Biol 53(3):383–397. doi:10.1023/B:PLAN.0000006944.61384.11

    Article  CAS  PubMed  Google Scholar 

  27. Ohnishi T, Sugahara S, Yamada T, Kikuchi K, Yoshiba Y, Hirano H-Y, Tsutsumi N (2005) OsNAC6, a member of the NAC gene family, is induced by various stresses in rice. Genes Genet Syst 80(2):135–139. doi:10.1266/ggs.80.135

    Article  CAS  PubMed  Google Scholar 

  28. Jensen MK, Rung JH, Gregersen PL, Gjetting T, Fuglsang AT, Hansen M, Joehnk N, Lyngkjaer MF, Collige DB (2007) The HvNAC6 transcription factor: a positive regulator of penetration resistance in barley and Arabidopsis. Plant Mol Biol 65:137–150. doi:10.1007/s11103-007-9204-5

    Article  CAS  PubMed  Google Scholar 

  29. Lin R, Zhao W, Meng X, Wang M, Peng Y (2007) Rice gene OsNAC19 encodes a novel NAC-domain transcription factor and responds to infection by Magnaporthe grisea. Plant Sci 172:120–130. doi:10.1016/j.plantsci.2006.07.019

    Article  CAS  Google Scholar 

  30. Takashi K, Taga Y, Takai R, Iwano M, Mastsui H, Takayama S, Isogai A, Che FS (2009) The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death. EMBO J 28:926–936. doi:10.1038/emboj.2009.39

    Article  Google Scholar 

  31. Xie Q, Sanz-Burgos AP, Guo H, García JA, Gutiérrez C (1999) GRAB proteins, novel members of the NAC domain family, isolated by their interaction with a geminivirus protein. Plant Mol Biol 39:647–656. doi:10.1023/A:1006138221874

    Article  CAS  PubMed  Google Scholar 

  32. Xue GP, Bower NI, McIntyre CL, Riding GA, Kazan K, Shorter R (2006) TaNAC69 from NAC superfamily of transcription factors is up-regulated by abiotic stresses in wheat and recognises two consensus DNA-binding sequences. Funct Plant Biol 33:43–57. doi:10.1071/FP05161

    Article  CAS  Google Scholar 

  33. Uauy C, Distelfeld A, Fahima T, Blechl AE, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314:1298–1301

    Article  CAS  PubMed  Google Scholar 

  34. Chen XM (2005) Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] on wheat. Can J Plant Pathol 27:314–337

    Article  Google Scholar 

  35. Stakman EC, Stewart DM, Loegering WQ (1962) Identification of physiological races of Puccinia graminis var. tritici. US Department of Agriculture, Agric Res Serv E-617

  36. Kang ZS, Li ZQ (1984) Discovery of a normal T type new pathogenic strain to Lovrin10. Acta Cllegii Septentrionali Occidentali Agriculturae 4:18–28

    Google Scholar 

  37. Zhang G, Dong YL, Zhang Y, Li YM, Wang XJ, Han QM, Huang LL, Kang Zhensheng (2009) Cloning and characterization of a novel hypersensitive-induced reaction gene from wheat infected by stripe rust pathogen. J Phytopathol 157:722–728. doi:10.1111/j.1439-0434.2009.01550

    Article  CAS  Google Scholar 

  38. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  CAS  PubMed  Google Scholar 

  39. Kozak M (1987) An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res 15:8125–8148

    Article  CAS  PubMed  Google Scholar 

  40. Kozak M (1990) Downstream secondary structure facilitates recognition of initiator codons by eukaryotic ribosomes. Proc Natl Acad Sci USA 87:8301–8305

    Article  CAS  PubMed  Google Scholar 

  41. Kikuchi K, Ueguchi-Tanaka M, Yoshida KT, Nagato Y, Matsusoka M, Hirano HY (2000) Molecular analysis of the NAC gene family in rice. Mol Gen Genet 262:1047–1051. doi:10.1007/PL00008647

    Article  CAS  PubMed  Google Scholar 

  42. Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, Hayashihide Y, Suzuki K, Kojima K, Takahara Y, Yamamoto K, Kikuchi S (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247. doi:10.1093/dnares/10.6.239

    Article  CAS  PubMed  Google Scholar 

  43. Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LSP, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876. doi:10.1111/j.1365-313X.2004.02171.x

    Article  CAS  PubMed  Google Scholar 

  44. Meng Q, Zhang C, Gai J, Yu D (2007) Molecular cloning, sequence characterization and tissue-specific expression of six NAC-like genes in soybean [Glycine max (L.) Merr.]. J Plant Physiol 164:1002–1012

    Article  CAS  PubMed  Google Scholar 

  45. Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3 are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19:270–280

    Article  CAS  PubMed  Google Scholar 

  46. Yoo YS, Kim Y, Kim SY, Lee JS, Ahn JH (2007) Control of Flowering time and cold response by a NAC-domain protein in Arabidopsis. PLoS ONE 2:e642. doi:10.1371/journal.pone.0000642.g001

    Article  PubMed  Google Scholar 

  47. Lam-Son PT, Quach TN, Guttikonda SK, Aldrich DL, Kumar R, Neelakandan A, Valliyodan B, Nguyen HT (2009) Molecular characterization of stress-inducible GmNAC genes in soybean. Mol Genet Genomics 281:647–664. doi:10.1007/s00438-009-0436-8

    Article  Google Scholar 

  48. Lamb CJ, Lawton MA, Dron M, Dixon RA (1989) Signal and transduction mechanisms for activation of plant defenses against microbial attack. Cell 56:215–224

    Article  CAS  PubMed  Google Scholar 

  49. Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178

    Article  CAS  PubMed  Google Scholar 

  50. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479

    Article  CAS  PubMed  Google Scholar 

  51. Wang CF, Huang LL, Buchenauer H, Han QM, Zhang HC, Kang ZS (2007) Histochemical studies on the accumulation of reactive oxygen species (O2 and H2O2) in the incompatible and compatible interaction of wheat-Puccinia striiformis f. sp. tritici. Physiol and Mol Plant Pathol 71:230–239. doi:10.1016/j.pmpp.2008.02.006

    Article  CAS  Google Scholar 

  52. Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr Opin Plant Biol 4:301–308. doi:10.1016/S1369-5266(00)00177-1

    Article  CAS  PubMed  Google Scholar 

  53. McGrath KC, Dombrecht B, Manners JM, Schenk PM, Edgar CI, Maclean DJ, Scheible WR, Udvardi MK, Kazan K (2005) Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol 139:949–959. doi:10.1104/pp.105.068544

    Article  CAS  PubMed  Google Scholar 

  54. Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant-pathogen interactions. Curr Opin Plant Biol 8:409–414. doi:10.1016/j.pbi.2005.05.015

    Article  CAS  PubMed  Google Scholar 

  55. Oh S-K, Lee S, Yu SH, Choi D (2005) Expression of a novel NAC domain containing transcription factor (CaNAC1) is preferentially associated with incompatible interactions between chili pepper and pathogens. Planta 222:876–887. doi:10.1007/s00425-005-0030-1

    Article  CAS  PubMed  Google Scholar 

  56. Carrera E, Prat S (1998) Expression of the Arabidopsis abi1-1 mutant allele inhibits proteinase inhibitor wound-induction in tomato. Plant J 15:765–771. doi:10.1046/j.1365-313X.1998.00261.x

    Article  CAS  PubMed  Google Scholar 

  57. Birkenmeier GF, Ryan CA (1998) Wound signaling in tomato plants. Evidence that ABA is not a primary signal for defense gene activation. Plant Physiol 117:687–693

    Article  CAS  PubMed  Google Scholar 

  58. Mysorel KS, Crasta OR, Tuori RP, Folkerts O, Swirsky PB, Martin GB (2002) Comprehensive transcript profiling of Pto-and Prf-mediated host defense responses to infection by Pseudomonas syringae pv. tomato. Plant J 32:299–315. doi:10.1046/j.1365-313X.2002.01424.x

    Article  Google Scholar 

  59. Delessert C, Kazan K, Wilson IW, Straeten DVD, Manners J, Dennis ES, Dolferus R (2005) The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. Plant J 43:745–757. doi:10.1111/j.1365-313X.2005.02488.x

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by grants from the National Natural Science Foundation of China (No. 30930064 and No. 30800712), the National High Technology Research and Development Program of China (863 Program, No. 2006AA10A104), the earmarked fund for Modern Agro-industry Technology Research System,and the 111 Project from the Ministry of Education of China (B07049).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhen-Sheng Kang.

Additional information

Ning Xia and Gang Zhang contribute equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 90 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xia, N., Zhang, G., Liu, XY. et al. Characterization of a novel wheat NAC transcription factor gene involved in defense response against stripe rust pathogen infection and abiotic stresses. Mol Biol Rep 37, 3703–3712 (2010). https://doi.org/10.1007/s11033-010-0023-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-010-0023-4

Keywords

Navigation