Skip to main content
Log in

Genome-wide analysis, expression dynamics and varietal comparison of NAC gene family at various developmental stages in Morus notabilis

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

Abstract

NAC genes are important transcription factors and forms a large family in plants. They have shown to play an important role in growth and development and have also been shown to involve in regulation of stress-responsive genes. In the present study, a repertoire of NAC genes in recently published mulberry genome has been identified which consists of a total of 79 members. Structural analysis revealed that most of the NAC genes in mulberry contain two introns. The proteins encoded by them show a wide range of isoelectric points suggestive of their varied roles in varying microcellular environment. Phylogenetic and conserved motif analysis elucidate the presence of 15 sub-groups of these genes along with two novel sub-groups having distinct conserved motifs which are not present in Arabidopsis. Gene ontology term enrichment analysis and cis-element identification from their putative 1 K upstream regulatory region indicates their possible role in important biological processes like organ formation, meristem establishment, senescence, and various biotic and abiotic stresses. Expression analysis across various developmental stages led to identification of their preferential expression in diverse tissues. Taken together, this work provides a solid background information related to structure, function, expression and evolution of NAC gene family in mulberry.

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
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/

  • Andronis C, Barak S, Knowles SM, Sugano S, Tobin EM (2008) The clock protein CCA1 and the bZIP transcription factor HY5 physically interact to regulate gene expression in Arabidopsis. Mol Plant 1:58–67

    Article  PubMed  CAS  Google Scholar 

  • Babu AM, Kumar JS, Kumar V, Sarkar A, Datta RK (2002) Tropic failure of Phyllactinia corylea contributes to the mildew resistance of mulberry genotypes. Mycopathologia 156:207–213

    Article  PubMed  CAS  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cenci A, Guignon V, Roux N, Rouard M (2014) Genomic analysis of NAC transcription factors in banana (Musa acuminata) and definition of NAC orthologous groups for monocots and dicots. Plant Mol Biol 85:63–80

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chatterjee SN, Nagaraja GM, Srivastava PP, Naik G (2004) Morphological and molecular variation of Morus laevigata in India. Genetica 121:133–143

    Article  PubMed  CAS  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29:644

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Higo H (1998) PLACE: a database of plant cis-acting regulatory DNA elements. Nucleic Acids Res 26:358–359

    Article  PubMed  PubMed Central  CAS  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 10:1–23

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu W, Wei Y, Xia Z, Yan Y, Hou X, Zou M, Lu C, Wang W, Peng M (2015b) Genome-wide identification and expression analysis of the NAC transcription factor family in cassava. PLoS One 10:e0136993

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Itoh Y, Kitamura Y, Fukazawa C (1994) The glycinin box: a soybean embryo factor binding motif within the quantitative regulatory region of the 11S seed storage globulin promoter. Mol Gen Genet 243:353–357

    Article  PubMed  CAS  Google Scholar 

  • Jensen MK, Kjaersgaard T, Petersen K, Skriver K (2010) NAC genes. Plant Signal Behav 5:907–910

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ko J-H, Yang SH, Park AH, Lerouxel O, Han K-H (2007) ANAC012, a member of the plant-specific NAC transcription factor family, negatively regulates xylary fiber development in Arabidopsis thaliana. Plant J 50:1035–1048

    Article  PubMed  CAS  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323

    Article  CAS  Google Scholar 

  • Li T, Qi X, Zeng Q, Xiang Z, He N (2014) MorusDB: a resource for mulberry genomics and genome biology. Database 2014:bau054

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21:3448–3449

    Article  PubMed  CAS  Google Scholar 

  • Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39:D225–D229

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Müller M, Knudsen S (1993) The nitrogen response of a barley C-hordein promoter is controlled by positive and negative regulation of the GCN4 and endosperm box. Plant J Cell Mol Biol 4:343–355

    Article  Google Scholar 

  • Nakashima K, Tran L-SP, 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  PubMed  CAS  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 465:30–44

    Article  PubMed  CAS  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 

  • 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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sakuraba Y, Piao W, Lim J-H, Han S-H, Kim Y-S, An G, Paek N-C (2015) Rice ONAC106 inhibits leaf senescence and increases salt tolerance and tiller angle. Plant Cell Physiol 56:2325–2339

    Article  PubMed  Google Scholar 

  • Shang H, Li W, Zou C, Yuan Y (2013) Analyses of the NAC transcription factor gene family in Gossypium raimondii Ulbr.: chromosomal location, structure, phylogeny, and expression patterns. J Integr Plant Biol 55:663–676

    Article  PubMed  CAS  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  PubMed  PubMed Central  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  PubMed  CAS  Google Scholar 

  • Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, Dagdigian C, Fuellen G, Gilbert JGR, Korf I, Lapp H, Lehväslaiho H, Matsalla C, Mungall CJ, Osborne BI, Pocock MR, Schattner P, Senger M, Stein LD, Stupka E, Wilkinson MD, Birney E (2002) The Bioperl toolkit: Perl modules for the life sciences. Genome Res 12:1611–1618

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tikader A, Dandin SB (2005) Biodiversity, geographical distribution, utilization and conservation of wild mulberry Morus serrata Roxb. Casp J Environ Sci 3:179–186

    Google Scholar 

  • Tikader A, Kamble CK (2008) Mulberry wild species in India and their use in crop improvement a review. Aust J Crop Sci 2:64–72

    Google Scholar 

  • Wang N, Zheng Y, Xin H, Fang L, Li S (2012) Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep 32:61–75

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu C, Perry SE (2005) Control of expression and autoregulation of AGL15, a member of the MADS-box family. Plant J 41:583–594

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Research performed in this article has been supported by grants from Department of Biotechnology, Government of India to PK. The authors remain indebted to anonymous reviewers whose suggestions have greatly improved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paramjit Khurana.

Ethics declarations

Conflict of interest

Author 1 declares that he/she has no conflict of interest. Author 2 declares that he/she has no conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

438_2016_1186_MOESM1_ESM.eps

Supplementary Fig. S1 Word cloud for the cis-elements representing the most frequent cis-motif present in the putative promoters of NAC genes in Morus notabilis (EPS 1296 kb)

438_2016_1186_MOESM2_ESM.eps

Supplementary Fig. S2 Network of gene ontology enrichment analysis for biological process terms of NAC genes in Morus notabilis. Node size and color intensity represent their significance level (EPS 3511 kb)

438_2016_1186_MOESM3_ESM.xls

Supplementary data Table S1 Details of Morus NAC components and their properties including gene, mRNA and protein length, number of exons and introns etc (XLS 15 kb)

Supplementary data Table S2 Gene ontology enrichment analysis result for biological process terms (XLS 31 kb)

Supplementary data Table S3 Gene ontology enrichment analysis result for cellular component terms (XLS 8 kb)

Supplementary data Table S4 Gene ontology enrichment analysis result for molecular function terms (XLS 7 kb)

Supplementary data Table S5 TMM normalized FPKM values for NAC gene components across the seven stages (XLS 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baranwal, V.K., Khurana, P. Genome-wide analysis, expression dynamics and varietal comparison of NAC gene family at various developmental stages in Morus notabilis . Mol Genet Genomics 291, 1305–1317 (2016). https://doi.org/10.1007/s00438-016-1186-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-016-1186-z

Keywords

Navigation