Skip to main content
Log in

Identification of 32 full-length NAC transcription factors in ramie (Boehmeria nivea L. Gaud) and characterization of the expression pattern of these genes

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

NAM, ATAF, and CUC (NAC) genes are plant-specific transcription factors (TFs) that play key roles in plant growth, development, and stress tolerance. To date, none of the ramie NAC (BnNAC) genes had been identified, even though ramie is one of the most important natural fiber crops. In order to mine the BnNAC TFs and identify their potential function, the search for BnNAC genes against two pools of unigenes de novo assembled from the RNA-seq in our two previous studies was performed, and a total of 32 full-length BnNAC genes were identified in this study. Forty-seven function-known NAC proteins published in other species, in concert with these 32 BnNAC proteins were subjected to phylogenetic analysis, and the result showed that all the 79 NAC proteins can be divided into eight groups (NAC-I–VIII). Among the 32 BnNAC genes, 24, 2, and 1 gene showed higher expression in stem xylem, leaf, and flower, respectively. Furthermore, the expression of 14, 11 and 4 BnNAC genes was regulated by drought, cadmium stress, and infection by root lesion nematode, respectively. Interestingly, there were five BnNAC TFs which showed high homology with the NAC TFs of other species involved in regulating the secondary wall synthesis, and their expressions were not regulated by drought and cadmium stress. These results suggested that the BnNAC family might have a functional diversity. The identification of these 32 full-length BnNAC genes and the characterization of their expression pattern provide a basis for future clarification of their functions in ramie growth and development.

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

References

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Balazadeh S, Siddiquil H, Allu A, Matallana-Ramirez L, Caldana C, Mehrnia M, Zanor M, hler B, Mueller-Roeber B (2010) A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J 62:250–264

    Article  CAS  PubMed  Google Scholar 

  • Balazadeh S, Kwasniewski M, Caldana C, Mehrnia M, Zanor M, Xue G, Mueller-Roeber B (2011) ORS1, an H2O2-responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Mol Plant 4:346–360

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen J, Guo Q, Zhang X (2006) Cloning full length of Ramie Caffeoyl-CoA 3-O-methyltransferase cDNA and sequence analysis. Scientia Agricultura Sinica 39:1058–1063

    CAS  Google Scholar 

  • Ernst H, Olsen A, Larsen S, Leggio L (2004) Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep 5:297–303

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fang Y, You J, Xie K, Xie W, Xiong L (2006) Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genomics 280:547–563

    Article  Google Scholar 

  • Gao F, Xiong A, Peng R, Jin X, Xu J, Zhu B, Chen J, Yao Q (2010) OsNAC52, a rice NAC transcription factor, potentially responds to ABA and confers drought tolerance in transgenic plants. Plant Cell Tiss Organ Cult 100:255–262

    Article  CAS  Google Scholar 

  • Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hu R, Qi G, Kong Y, Kong D, Gao Q, Zhou G (2010) Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10:145

    Article  PubMed Central  PubMed  Google Scholar 

  • Ishida T, Aida M, Takada S, Tasaka M (2000) Involvement of CUPSHAPED COTYLEDON genes in gynoecium and ovule development in Arabidopsis thaliana. Plant Cell Physiol 41:60–67

    Article  CAS  PubMed  Google Scholar 

  • Jeong J, Kim Y, Baek K, Jung H, Ha S, Do Choi Y, Kim M, Reuzeau C, Kim J (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:187–195

    Google Scholar 

  • Jin J, Zhang H, Kong L, Gao G, Luo J (2013a) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res. doi:10.1093/nar/gkt1016

    Google Scholar 

  • Jin H, Huang F, Cheng H, Song H, Yu D (2013b) Overexpression of the GmNAC2 gene, an NAC transcription factor, reduces abiotic stress tolerance in Tobacco. Plant Mol Biol Rep 31:435–442

    Article  CAS  Google Scholar 

  • John I, Hackett R, Cooper W, Drake R, Farrell A, Grierson D (1997) Cloning and characterization of tomato leaf senescence-related cDNAs. Plant Mol Biol 33:641–651

    Article  CAS  PubMed  Google Scholar 

  • Kaneda T, Taga Y, Takai R, Iwano M, Matsui H, Takayama S, Isogai A, Che F (2009) The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death. EMBO J 28:926–936

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kato H, Motomura T, Komeda Y, Saito T, Kato A (2010) Overexpression of the NAC transcription factor family gene ANAC036 results in adwarf phenotype in Arabidopsis thaliana. J Plant Physiol 167:571–577

    Article  CAS  PubMed  Google Scholar 

  • Kim Y, Kim S, Park J, Park H, Lim M, Chua N, Parka C (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18:3132–3144

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kim S, Kim S, Park C (2007) A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta 226:647–654

    Article  CAS  PubMed  Google Scholar 

  • Kim M, Park M, Seo P, Song J, Kim H, Park C (2012) Controlled nuclear import of NTL6 transcription factor reveals a cytoplasmic role of SnRK2.8 in drought stress response. Biochem J 448:353–363

    Article  CAS  PubMed  Google Scholar 

  • Kou X, Watkins C, Gan S (2012) Arabidopsis AtNAP regulates fruit senescence. J Exp Bot 63:6139–6147

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kunieda T, Mitsuda N, Ohme-Takagi M, Takeda S, Aida M, Tasaka M, Kondo M, Nishimura M, Hara-Nishimura I (2008) NAC family proteins NARS1/NAC2 and NARS2/NAM in the outer integument regulate embryogenesis in Arabidopsis. Plant Cell 20:2631–2642

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee S, Seo P, Lee H, Park C (2012) A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J 70:831–844

    Article  CAS  PubMed  Google Scholar 

  • Li P, Windb J, Shi X, Zhang H, Hanson J, Smeekens S, Teng S (2011) Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain. Proc Natl Acad Sci USA 108:3436–3441

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li Q, Lina Y, Sun Y, Song J, Chen H, Zhang X, Sederoff R, Chiang V (2012) Splice variant of the SND1 transcription factor is a dominant negative of SND1 members and their regulation in Populus trichocarpa. Proc Natl Acad Sci USA 109:14699–14704

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu J, Yu C, Tang S, Zhu A, Wang Y, Zhu S, Ma X, Xiong H (2008) Cloning and tissue expression of important enzyme gene UGlcAE in ramie pectin biosynthesis. ACTA AGRONOMICA SINICA 34:1938–1945

    Article  CAS  Google Scholar 

  • Liu T, Zhu S, Tang Q, Chen P, Yu Y, Tang S (2013a) De novo assembly and characterization of transcriptome using Illumina paired-end sequencing and identification of CesA gene in ramie (Boehmeria nivea L.Gaud). BMC Genomics 14:125

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu T, Zhu S, Tang Q, Yu Y, Tang S (2013b) Identification of drought stress-responsive transcription factors in ramie (Boehmeria nivea L. Gaud). BMC Plant Biol 13:130

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Mao X, Zhang H, Qian X, Li A, Zhao G, Jing R (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 63:2933–2946

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickening and are required for anther dehiscence. Plant Cell 17:2993–3006

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mitsuda N, IwaseA 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 Central  PubMed  Google Scholar 

  • Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630

    Article  CAS  PubMed  Google Scholar 

  • Nuruzzaman M, Manimekalai R, Sharoni A, Satoh K, Kondoh H, Ooka H, Kikuchi S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30–44

    Article  CAS  PubMed  Google Scholar 

  • Olsen A, Ernst H, Leggio L, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87

    Article  CAS  PubMed  Google Scholar 

  • Park J, Kim Y, Kim S, Jung J, Woo J, Park C (2011) Integration of auxin and salt signals by the NAC transcription factor NTM2 during seed germination in Arabidopsis. Plant Physiol 156:537–549

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pinheiro G, Marques C, Costa M, Reis P, Alves M, Carvalho C, Fietto L, Fontes E (2009) Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 444:10–23

    Article  CAS  PubMed  Google Scholar 

  • 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 Central  PubMed  Google Scholar 

  • She W, Jie Y, Xing H, Luo Z, Kang W, Huang M, Zhu S (2011) Absorption and accumulation of cadmium by ramie (Boehmeria nivea) cultivars: a field study. ACTA AGR SCAND B-S P 61:641–647

    CAS  Google Scholar 

  • Souer E, van Houwelingen A, Kloos D, Mol J, Koes R (1996) The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 85:159–170

    Article  CAS  PubMed  Google Scholar 

  • Sun H, Huang X, Xu X, Lan H, Huang J, Zhang H (2012) ENAC1, a NAC transcription factor, is an early and transient response regulator induced by abiotic stress in rice (Oryza sativa L.). Mol Biotechnol 52:101–110

    Article  CAS  PubMed  Google Scholar 

  • Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics 284:173–183

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tian Z, Yi R, Chen J, Guo Q, Zhang X (2008) Cloning and expression of cellulose synthase gene in Ramie [Boehmeria nivea (Linn.) Gaud.]. ACTA AGRONOMICA SINICA 34:76–83

    CAS  Google Scholar 

  • Tran L, Nakashima K, Sakuma Y, Simpson S, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress inducible NAC transcription factors that bind to a drought responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vandesompele J, de Preter K, Pattyn F, Poppe B, Roy N, Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034

    Google Scholar 

  • Vroemen CW, Mordhorst AP, Albrecht C, Kwaaitaal MA, de Vries SC (2003) The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15:1563–1577

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu A, Allu A, Garapati P, Siddiqui H, Dortay H et al (2012) JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24:482–506

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xie Q, Sanz-Burgos A, Guo H, Garcia J, Gutierrez 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

    Article  CAS  PubMed  Google Scholar 

  • Xie Q, Frugis G, Colgan D, Chua N (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid–inducible mitogen-activated protein Kinase. Plant Cell 15:745–759

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamaguchi M, Mitsuda N, Ohtani M, Ohme-Takagi M, Kato K, Demura T (2011) VASCULAR-RELATED NAC-DOMAIN 7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J 66:579–590

    Article  CAS  PubMed  Google Scholar 

  • Yang B, Zhou M, Shu W, Lan C, Ye Z, Qiu R, Jie Y, Cui G, Wong M (2010) Constitutional tolerance to heavy metals of a fiber crop, ramie (Boehmeria nivea), and its potential usage. Environ Pollut 158:551–558

    Article  CAS  PubMed  Google Scholar 

  • Yang S, Seo P, Yoon H, Park C (2011) The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23:2155–2168

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yoshii M, Shimizu T, Yamazaki M, Higashi T, Miyao A, Hirochika H, Omura T (2009) Disruption of a novel gene for a NAC-domain protein in rice confers resistance to Rice dwarf virus. Plant J 57:615–625

    Article  CAS  PubMed  Google Scholar 

  • Ze´licourt A, Diet A, Marion J, Laffont C, Ariel F, Moison M, Zahaf O, Crespi M, Gruber V, Frugier F (2012) Dual involvement of a Medicago truncatula NAC transcription factor in root abiotic stress response and symbiotic nodule senescence. Plant J 70:220–230

    Article  Google Scholar 

  • Zhao C, Avci U, Grant E, Haigler C, Beers E (2008) XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem. Plant J 53:425–436

    Article  CAS  PubMed  Google Scholar 

  • Zheng X, Chen B, Lu G, Han B (2009) Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem Biophy Res Commun 379:985–989

    Article  CAS  Google Scholar 

  • Zhong R, Lee C, Ye Z (2010) Functional characterization of poplar wood associated NAC domain transcription factors. Plant Physiol 152:1044–1055

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu Q, Huang D, Liu S, Luo Z, Rao Z, Cao X, Ren X (2013) Accumulation and subcellular distribution of cadmiumin ramie (Boehmeria nivea L. Gaud.). Plant Soil Environ 59:57–61

    CAS  Google Scholar 

  • Zhu S, Tang S, Tang Q and Liu T (2014) Genome-wide transcriptional changes of ramie (Boehmeria nivea L.Gaud) in response to the infection of root-lesion nematode. BMC Genomics (in press)

Download references

Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (31101189, 31201172) and the National Modern Agro-industry Technology Research System (nycytx-19-E16). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Touming Liu.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, T., Zhu, S., Tang, Q. et al. Identification of 32 full-length NAC transcription factors in ramie (Boehmeria nivea L. Gaud) and characterization of the expression pattern of these genes. Mol Genet Genomics 289, 675–684 (2014). https://doi.org/10.1007/s00438-014-0842-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-014-0842-4

Keywords

Navigation