Abstract
The NAC (NAM, ATAF and CUC) proteins are plant-specific transcription factors implicated in development and stress responses. In the present study 88 pigeonpea NAC genes were identified from the recently published draft genome of pigeonpea by using homology based and de novo prediction programmes. These sequences were further subjected to phylogenetic, motif and promoter analyses. In motif analysis, highly conserved motifs were identified in the NAC domain and also in the C-terminal region of the NAC proteins. A phylogenetic reconstruction using pigeonpea, Arabidopsis and soybean NAC genes revealed 33 putative stress-responsive pigeonpea NAC genes. Several stress-responsive cis-elements were identified through in silico analysis of the promoters of these putative stress-responsive genes. This analysis is the first report of NAC gene family in pigeonpea and will be useful for the identification and selection of candidate genes associated with stress tolerance.
Similar content being viewed by others
References
Vavilov NI (1951) The origin, variation, immunity, and breeding of cultivated plants. Chron Bot 13:1–366
De DN (1974) Pigeonpea. In: Hutchinson J (ed) Evolutionary studies in world crops: diversity and change in the Indian subcontinent. Cambridge University Press, London, pp 79–87
Royes WV (1976) Pigeon pea. In: Simmonds NW (ed) Evolution of Crop Plants. Longmans, London and New York
Singh NK, Gupta DK, Jayaswal PK, Mahato MK, Dutta S, Singh S, Bhutani S et al (2012) The first draft of the pigeonpea genome sequence. J Plant Biochem Biotechnol 21:98–112
Varshney RK, Chen W, Li Y, Bharti AK, Saxena RK, Schlueter JA, Donoghue MT, Azam S, Fan G, Whaley AM, Farmer AD, Sheridan J, Iwata A, Tuteja R, Penmetsa RV, Wu W, Upadhyaya HD, Yang SP, Shah T, Saxena KB, Michael T, McCombie WR, Yang B, Zhang G, Yang H, Wang J, Spillane C, Cook DR, May GD, Xu X, Jackson SA (2012) Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat Biotechnol 30:83–89
Prud’homme B, Gompel N, Rokas A, Kassner VA, Williams TM, Yeh SD, True JR, Carroll SB (2006) Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature 440:1050–1053
Tuch BB, Li H, Johnson AD (2008) Evolution of eukaryotic transcription circuits. Science 319:1797–1799
Zhang Y, Wang L (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol. doi:10.1186/1471-2148-5-1
Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110
Gutiérrez RA, Green PJ, Keegstra K, Ohlrogge JB (2004) Phylogenetic profiling of the Arabidopsis thaliana proteome: what proteins distinguish plants from other organisms? Genome Biol 5:R53
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
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
Hibara K, Takada S, Tasaka M (2003) CUC1 gene activates the expression of SAM-related genes to induce adventitious shoot formation. Plant J 36:687–696
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
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
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
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 46:521–529
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
Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signalling pathway. Plant J 39:863–876
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
Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87
Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381
Kikuchi K, Ueguchi-Tanaka M, Yoshida TK, Nagato Y, Matsusoka M, Hirano HY (1999) Molecular analysis of the NAC gene family in rice. Mol Gen Genet 262:1047–1051
Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, OsatoN KJ, 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
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
Pinheiro GL, Marques CS, Costa MD, Reis PA, Alves MS, Carvalho CM, Fietto LG, Fontes EP (2009) Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 444:10–23
Rushton PJ, Bokowiec MT, Han S, Zhang H, Brannock JF, Chen X, Laudeman TW, Timko MP (2008) Tobacco transcription factors: novel insights into transcriptional regulation in the solanaceae. Plant Physiol 147:280–295
Christiansen MW, Holm PB, Gregersen PL (2011) Characterization of barley (Hordeum vulgare L.) NAC transcription factors suggest conserved functions compared to both monocots and dicots. BMC Res Notes 4:302
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 Genomics 280:547–563
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 465:30–44
Wang N, Zheng Y, Xin H, Fang L, Li S (2013) Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep 32:61–75
Shen H, Yin YB, Chen F, Xu Y, Dixon RA (2009) A bioinformatic analysis of NAC genes for plant cell wall development in relation to lignocellulosic bioenergy production. Bioenergy Res 2:217–232
Yao D, Wei Q, Xu W, Syrenne RD, Yuan JS, Su Z (2012) Comparative genomic analysis of NAC transcriptional factors to dissect the regulatory mechanisms for cell wall biosynthesis. BMC Bioinform 13:S10
Stanke M, Steinkamp R, Waack S, Morgenstern B (2004) AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res 32:W309–W312
Besemer J, Borodovsky M (2005) GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res 33:W451–W454
Burge C, Karlin S (1997) Prediction of complete gen structures in human genomic DNA. J Mol Biol 268:78–94
Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunesekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Research Database Issue 38:D211–D222
Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95:5857–5864
Dutta S, Kumawat G, Singh BP, Gupta DK, Singh S, Dogra V, Gaikwad K, Sharma TR, Raje RS, Bandhopadhya TK, Datta S, Singh MN, Bashasab F, Kulwal P, Wanjari KB, Varshney RK, Cook DR, Singh NK (2011) Development of genic-SSR markers by deep transcriptome sequencing in pigeonpea [Cajanus cajan (L.) Millspaugh]. BMC Plant Biol 11:17
Perez-Rodriguez P, Riano-Pachon DM, Correa LGG, Rensing SA, Kersten B, Mueller-Roeber B (2009) PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38:D822–D827
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066
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
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34(Web Server issue):W369–W373
Zdobnov EM, Apweiler R (2001) InterProScan—an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848
Jensen MK, Kjaersgaard T, Nielsen MM, Galberg P, Petersen K, O’Shea C, Skriver K (2010) The Arabidopsis thaliana NAC transcription factor family: structure-function relationships and determinants of ANAC019 stress signaling. Biochem J 426:183–196
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
Zhu T, Nevo E, Sun D, Peng J (2012) Phylogenetic analyses unravel the evolutionary history of NAC proteins in plants. Evolution 66:1833–1848
Zhang G, Chen M, Chen X, Xu Z, Guan S, Li L-C, Li A, Guo J, Mao L, Ma Y (2008) Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J Exp Bot 59:4095–4107
Mochida K, Yoshida T, Sakurai T, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2010) Genome-wide analysis of two-component systems and prediction of stress-responsive two-component system members in soybean. DNA Res 17:303–324
Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17:172–179
Singh AK, Sharma V, Pal AK, Acharya V, Ahuja PS (2013) Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.). DNA Res 20:403–423
Seo PJ, Park CM (2010) A membrane-bound NAC transcription factor as an integrator of biotic and abiotic stress signals. Plant Signal Behav 5(5):481–483
Kim SG, Kim SY, Park CM (2007) A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta 226:647–654
Kim SG, Lee AK, Yoon HK, Park CM (2008) A membrane-bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling in Arabidopsis seed germination. Plant J 55:77–78
Lee S, Seo PJ, Lee HJ, Park CM (2012) A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J 70:831–844
Kim YS, Kim SG, Park JE, Park HY, Lim MH, Chua NH, Park CM (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18:3132–3144
Yoshiyama K, Conklin PA, Huefner ND, Britt AB (2009) Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage. Proc Natl Acad Sci USA 106:12843–12848
Ernst HA, Olsen AN, Larsen S, Lo-Leggio L (2004) Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep 5:297–303
Zhao C, Avci U, Grant EH, Haigler CH, Beers EP (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
Yamaguchi M, Mitsuda N, Ohtani M, Ohme-Takagi M, Kato K, Demura T (2011) VASCULAR-RELATED NAC-DOMAIN7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J 66:579–590
Ohtani M, Nishikubo N, Xu B, Yamaguchi M, Mitsuda N, Goue N, Shi F, Ohme-Takagi M, Demura T (2011) A NAC domain protein family contributing to the regulation of wood formation in poplar. Plant J 67:499–512
Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206
Zahn LM, Kong H, Leebens-Mack JH, Kim S, Soltis PS, Landherr LL, Soltis DE, Depamphilis CW, Ma H (2005) The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169:2209–2223
Mundy J, Yamaguchi-Shinozaki K, Chua NH (1990) Nuclear proteins bind conserved elements in the abscisic acid-responsive promoter of a rice rab gene. Proc Natl Acad Sci USA 87:1406–1410
Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29 gene in response to dehydration and high-salinity stresses. Plant J 34:137–148
Mikkelsen MD, Thomashow MF (2009) A role for circadian evening elements in cold-regulated gene expression in Arabidopsis. Plant J 60:328–339
Acknowledgments
We thank the Indian Council of Agricultural Research (ICAR), New Delhi, India for funding this work through the Network Project on Transgenics in Crops (NPTC). VS and PTKJ thank the Indian Agricultural Research Institute (IARI) for the Senior Research Fellowship. PC gratefully acknowledges the Senior Research Fellowship awarded by the Council of Scientific and Industrial Research (CSIR). The authors also gratefully acknowledge the critical comments of the reviewer.
Author information
Authors and Affiliations
Corresponding author
Additional information
Viswanathan Satheesh, P Tej Kumar Jagannadham and Parameswaran Chidambaranathan have contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
11033_2014_3669_MOESM3_ESM.jpg
Supplementary Fig. 2 Phylogenetic reconstruction of Arabidopsis, soybean and pigeonpea NAC transcription factors using the Neighbor-joining method in MEGA5. (JPG 1,415 kb)
11033_2014_3669_MOESM4_ESM.jpg
Supplementary Fig. 3 Pigeonpea NAC genes containing transmembrane domain in the C-terminal region indicated as TM, NAC represents NAC domain. The TM is identified utilizing (http://aramemnon.botanik.uni-koeln.de) analysis tool. (JPG 719 kb)
Rights and permissions
About this article
Cite this article
Satheesh, V., Jagannadham, P.T.K., Chidambaranathan, P. et al. NAC transcription factor genes: genome-wide identification, phylogenetic, motif and cis-regulatory element analysis in pigeonpea (Cajanus cajan (L.) Millsp.). Mol Biol Rep 41, 7763–7773 (2014). https://doi.org/10.1007/s11033-014-3669-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-014-3669-5