Skip to main content
SpringerLink
Log in

Evaluation of the diversity and phylogenetic implications of NAC transcription factor members of four reference species from the different embryophytic plant groups

  • Research Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

NAC transcription factors (TFs) are one of the largest and important TF family that are involved in the regulation of plant growth and development. They are characterized by a highly conserved N-terminal domain and a variable C-terminal domain. In the present study, the amino acid sequences of NAC TFs from four embryophytic plant species viz. Arabidopsis thaliana (Angiosperm), Picea abies (Gymnosperm), Selaginella moellendorffii (Pteridophyte) and Physcomitrella patens (Bryophyte) as reference of the different plant groups were collected from the Plant Transcription Factor Database (PTFD) and the phylogenetic relationships were evaluated. The phylogenetic tree revealed that the majority of the NAC members were interspersed in the major subgroups that indicated the expansion of the NAC members predates the speciation events. Thirty one (31), five (05), one (1) and ten (10) paralog pairs were determined respectively for Arabidopsis, Picea, Selaginella and Physcomitrella. The structure–function relationship of paralog pairs were inferred from the phylogenetic tree of combined set of paralogous gene pairs by studying the prevalence of flanking regions and motif analysis of the NAC proteins. The motif analysis revealed the presence of an N-terminal conserved domain, a characteristic of the majority of NAC family proteins. Conserved motifs in the C-terminal region were absent in the majority of the protein sequences except few members in Arabidopsis and Physcomitrella. Also the time of gene duplication of the paralog pairs were calculated that revealed the duplication events occurred between 4.48 and 45.94 MYA Arabidopsis, 167.57–532.86 MYA in Picea, and 29.12–53.53 MYA in Physcomitrella.

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

Access this article

Log in via an institution

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

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(6):841–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arsovski AA, Pradinuk J, Guo XQ, Wang S, Adams KL (2015) Evolution of cis-regulatory elements and regulatory networks in duplicated genes of Arabidopsis. Plant Physiol 169(4):2982–2991

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banks JA (2009) Selaginella and 400 million years of separation. Annu Rev Plant Biol 60:223–238

    Article  CAS  PubMed  Google Scholar 

  • Beilstein MA, Nagalingum NS, Clements MD, Manchester SR, Mathews S (2010) Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. PNAS 107(43):18724–18728

    Article  PubMed  PubMed Central  Google Scholar 

  • Bilas R, Szafran K, Hnatuszko-Konka K, Kononowicz AK (2016) Cis-regulatory elements used to control gene expression in plants. Plant Cell Tiss Org 127(2):269–287

    Article  CAS  Google Scholar 

  • Buschiazzo E, Ritland C, Bohlmann J, Ritland K (2012) Slow but not low: genomic comparisons reveal slower evolutionary rate and higher dN/dS in conifers compared to angiosperms. BMC Evol Biol 12:8

    Article  PubMed  PubMed Central  Google Scholar 

  • De Clercq I, Vermeirssen V, Van Aken O, Vandepoele K, Murcha MW, Law SR, Inze A, Ng S, Ivanova A, Rombaut D, Van de Cotte B, Jaspers P, Van de Peer Y, Kangasjarvi J, Whelan J, Van Breusegem F (2013) The membrane bound NAC transcription factor ANAC013 is a regulator of mitochondrial retrograde regulation of the oxidative stress response in Arabidopsis. Plant Cell 25(9):3472–3490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fang Y, You J, Xie K, Xie W, Xiong L (2008) Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genom 280:535–546

    Article  CAS  Google Scholar 

  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151(4):1531–1545

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hernandez-Garcia CM, Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Sci 217–218:109–119

    Article  CAS  PubMed  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27(1):297–300

    Article  CAS  PubMed  PubMed Central  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 103:12987–12992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297

    Article  PubMed  Google Scholar 

  • Hu W, Yang H, Yan Y, Wei Y, Tie W, Ding Z, Zuo J, Peng M, Kaimian L (2016) Genome-wide characterization and analysis of bZIP transcription factor gene family related to abiotic stress in cassava. Sci Rep 6:22783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes AL, Friedman R (2003) Parallel evolution by gene duplication in the genomes of two unicellular fungi. Genome Res 13(5):794–799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jensen MK, Rung JH, Gregersen PL, Gjetting T, Fuglsang AT, Hansen M, Joehnk N, Lyngkjaer MF, Collinge DB (2007) The HvNAC6 transcription factor: a positive regulator of penetration resistance in barley and Arabidopsis. Plant Mol Biol 65(1–2):137–150

    Article  CAS  PubMed  Google Scholar 

  • Jensen MK, Kjaersgaard T, Petersen K, Skriver K (2010) NAC genes: time-specific regulators of hormonal signaling in Arabidopsis. Plant Signal Behav 5(7):907–910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong JS, Kim YS, Baek KH, Jung H, Ha S-H, Choi YD, Kim M, Reuzeau C, Kim J-K (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153(1):185–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin JP, Zhang H, Kong L, Gao G, Luo JC (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42(D1):182–187

    Article  CAS  Google Scholar 

  • Keeley JE (2012) Ecology and evolution of pine life histories. Ann For Sci 69(4):445–453

    Article  Google Scholar 

  • Kenrick P (2000) The relationships of vascular plants. Phil Trans R Soc Lond B 355:847–855

    Article  CAS  Google Scholar 

  • Kikuchi S (2014) Genome-wide view of the expression profiles of NAC-domain genes in response to infection by rice viruses. In: Benkeblia N (ed) Omics technologies and crop improvement. CRC Press, Baca Raton, pp 127–152

    Chapter  Google Scholar 

  • Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498

    Article  CAS  PubMed  Google Scholar 

  • Kong H, Landherr LL, Frohlich MW, Leebens-Mack J, Ma H, de Pamphilis CW (2007) Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J 50:873–885

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2011) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 18:263–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li WH, Gojobori T (1983) Rapid evolution of goat and sheep globin genes following gene duplication. Mol Biol Evol 1(1):94–108

    CAS  PubMed  Google Scholar 

  • Li J, Yuan J, Li M (2014) Characterization of putative cis-regulatory elements in genes preferentially expressed in Arabidopsis male meiocytes. BioMed Res Int 2014: Article ID 708364

  • Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43:D222–D226

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97–103

    Article  CAS  PubMed  Google Scholar 

  • Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, Ooka H, Kikuchi S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465(1–2):30–44

    Article  CAS  PubMed  Google Scholar 

  • Nuruzzaman M, Sharoni AM, Kikuchi S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol 4:248

    Article  PubMed  PubMed Central  Google Scholar 

  • Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10(2):79–87

    Article  CAS  PubMed  Google Scholar 

  • Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, Hayashizaki 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

    Article  CAS  PubMed  Google Scholar 

  • Pascual MB, Canovas FM, Avila C (2015) The NAC transcription factor family in maritime pine (Pinus Pinaster): molecular regulation of two genes involved in stress responses. BMC Plant Biol 15:254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinheiro GL, Marques CS, Costa MDBL, Reis PAB, Alves MS, Carvalho CM, Fietto LG, Fontes EPB (2009) Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 444(1–2):10–23

    Article  CAS  PubMed  Google Scholar 

  • Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17(6):369–381

    Article  CAS  PubMed  Google Scholar 

  • Rensing SA, Ick J, Fawcett JA, Lang D, Zimmer A, Van de Peer Y, Reski R (2007) An ancient genome duplication contributed to the abundance of metabolic genes in the moss Physcomitrella patens. BMC Evol Biol 7:130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rensing SA, Ick J, Fawcett JA, Lang D, Zimmer A, Van de Peer Y, Reski R (2016) Erratum to: an ancient genome duplication contributed to the abundance of metabolic genes in the moss Physcomitrella patens. BMC Evol Biol 16:184

    Article  PubMed  PubMed Central  Google Scholar 

  • Schaefer DG, Zryd J-P (2001) The moss Physcomitrella patens, now and then. Plant Physiol 127(4):1430–1438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao H, Wang H, Tang X (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front Plant Sci 6:902

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen H, Yin Y, Chen F, Xu Y, Dixon RA (2009) A bioinformatic analysis of NAC genes for plant cell wall development in relation to lignocellulosic bioenergy production. Bioenerg Res 2:217–232

    Article  Google Scholar 

  • Singh LN, Hannenhalli S (2008) Functional diversification of paralogous transcription factors via divergence in DNA binding site motif and in expression. PLoS ONE 3(6):e2345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solovyev VV, Shahmuradov IA, Salamov AA (2010) Identification of promoter regions and regulatory sites. Method Mol Biol 674:57–83

    Article  CAS  Google Scholar 

  • Soltis PS, Soltis DE (2013) A conifer genome spruces up plant phylogenomics. Genome Biol 14(6):122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Souer E, Van Houwelingen A, Kloos D, Mol JNM, 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 

  • Su H, Zhang S, Yuan X, Chen C, Wang XF, Hao YJ (2013) Genome-wide analysis and identification of stress-responsive genes of the NAM-ATAF1, 2-CUC2 transcription factor family in apple. Plant Physiol Biochem 71:11–21

    Article  CAS  PubMed  Google Scholar 

  • Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609–W612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tran LS, Nakashima K, Sakuma Y, Simpson SD, 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  PubMed Central  Google Scholar 

  • Tran LS, Nishiyama R, Yamaguchi-Shinozaki K, Shinozaki K (2010) Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach. GM Crops 1:32–39

    Article  PubMed  Google Scholar 

  • Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314(5803):1298–1301

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • Yang X, Tuskan GA, Cheng MZ (2006) Divergence of the Dof gene families in poplar, Arabidopsis, and rice suggests multiple modes of gene evolution after duplication. Plant Physiol 142:820–830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Zhou Y, Wang X, Gu S, Yu J, Liang G, Yan C, Xu C (2008) Genomewide comparative phylogenetic and molecular evolutionary analysis of tubby-like protein family in Arabidopsis, rice, and poplar. Genomics 92:246–253

    Article  CAS  PubMed  Google Scholar 

  • Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18(6):292–298

    Article  Google Scholar 

  • Zhu T, Nevo E, Sun D, Peng J (2012) Phylogenetic analyses unravel the evolutionary history of NAC proteins in plants. Evolution 66(6):1833–1848

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The corresponding author is grateful to Dr. Vinay Singh, Information Officer, Centre for Bioinformatics, Banaras Hindu University, Varanasi, India for providing valuable inputs for the present study. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

  1. Department of Botany, A.P.C. Roy Govt. College, Matigara, Siliguri, WB, 734010, India

    Rakhi Chakraborty

  2. Molecular and Analytical Biochemistry Laboratory, Department of Botany, University of Gour Banga, Mokdumpur, Malda, WB, 732103, India

    Swarnendu Roy

Authors
  1. Rakhi Chakraborty
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Swarnendu Roy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Swarnendu Roy.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chakraborty, R., Roy, S. Evaluation of the diversity and phylogenetic implications of NAC transcription factor members of four reference species from the different embryophytic plant groups. Physiol Mol Biol Plants 25, 347–359 (2019). https://doi.org/10.1007/s12298-018-0581-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-018-0581-9

Keywords

Search

Navigation