Skip to main content
SpringerLink
Log in

Genome-wide identification, classification and expression analysis of NAC family of genes in sorghum [Sorghum bicolor (L.) Moench]

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

NAC transcription factors are involved in many biological processes via regulation of downstream target gene expression and play essential roles in regulation of plant growth and improving plant tolerance to abiotic stress. NAC transcription factors have been studied in various species, but little information is available regarding these factors in sorghum. Genome-wide investigation of potentially abiotic stress related sorghum NAC-type genes was performed. A total of 145 non-redundant NAC genes (SbNAC1 –SbNAC145) were identified in the sorghum genome. These genes were distributed unevenly across the 10 chromosomes, and were divided into 16 groups based on sequence similarity. Gene structure analysis indicated that most SbNAC genes contained three exons and two introns, and had ten putative conserved motifs. Phylogenetic analysis indicated that the SbNAC genes with similar motif distributions were clustered into the same branch. Seven SbNAC genes, which were grouped into the stress-related subgroup, were isolated and have been confirmed to have transcriptional activity in yeast. SbNAC genes showed differential expression patterns over time in response to dehydration, salinity, cold, and phytohormone abscisic acid stress treatments, thus suggesting essential roles in plant responses to abiotic stress. In the germination stage, SbNAC56 overexpression transgenic lines exhibited significantly enhanced hypersensitivities to ABA, NaCl and d-Mannitol. This may infer that SbNAC56 may play essential roles in plants response to abiotic stresses in ABA dependent signaling pathway. Here, we present a comprehensive overview of the SbNAC genes and provide a foundation for future functional research regarding their biological roles in sorghum stress tolerance, even in the regulation of plant growth.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

NAC :

NAM, ATAF and CUC transcription factor

TF :

Transcription factor

TM :

Transmembrane

qRT-PCR :

Quantitative real-time polymerase chain reaction

SD :

Synthetic dropout

Chr :

Chromosomes

References

  • Baloglu MC, Oz MT, Oktem HA et al (2012) Expression analysis of TaNAC69-1 and TtNAMB-2, wheat NAC family transcription factor genes under abiotic stress conditions in durum wheat (Triticum turgidum). Plant Mol Biol Rep 30:1246–1252

    Article  CAS  Google Scholar 

  • Broun P (2004) Transcription factors as tools for metabolic engineering in plants. Curr Opin Plant Biol 7:202–209

    Article  CAS  PubMed  Google Scholar 

  • Endre A, Bantte K (2017) Evaluation and association mapping of agronomic traits for drought tolerance in sorghum [Sorghum bicolor (L.) Moench]. Afr J Biotechnol 16:631–642

    Article  Google Scholar 

  • Guo YF, Gan SS (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612

    Article  CAS  PubMed  Google Scholar 

  • Guo HS, Xie Q, Fei JF (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to down regulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–1386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo WW, Zhang JX, Zhang N et al (2015) The wheat NAC transcription factor TaNAC2L is regulated at the transcriptional and post-translational levels and promotes heat stress tolerance in transgenic Arabidopsis. PloS ONE 10:e0135667

    Article  PubMed  PubMed Central  Google Scholar 

  • Hao YJ, Wei W, Song QX et al (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68:302–313

    Article  CAS  PubMed  Google Scholar 

  • He XJ, Mu RL, Cao WH et al (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916

    Article  CAS  PubMed  Google Scholar 

  • Hu RB, Qi G, Kong YZ et al (2010) Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10:1–23

    Article  Google Scholar 

  • Ji L, Hu RB, Jiang JX et al (2014) Molecular cloning and expression analysis of 13 NAC transcription factors in Miscanthus lutarioriparius. Plant Cell Rep 33:2077–2092

    Article  CAS  PubMed  Google Scholar 

  • Jin L, Tran DQ, McLachlan JA et al (1997) Several synthetic chemicals inhibit progesterone receptor-mediated transactivation in yeast. Biochem Biophys Res Commun 233:139–146

    Article  CAS  PubMed  Google Scholar 

  • Jing L, Guo G, Guo W et al (2012) miRNA164-directed cleavage of ZmNAC1 confers lateral root development in maize (Zea mays L.). BMC Plant Biol 12:220

    Article  Google Scholar 

  • Kebede H, Subudhi PK, Rosenow DT et al (2001) Quantitative trait loci influencing drought tolerance in grain sorghum (Sorghum bicolor L. Moench). Theor Appl Genet 103:266–276

    Article  CAS  Google Scholar 

  • Li B, Ni ZY, Li XD et al (2012) Construction of prokaryotic expression vector, protein purification and identification of GhCOMT1 gene from Gossypium hirsutum L. Acta Bot Boreali-Occidential Sinica 32:1971–1976

    CAS  Google Scholar 

  • Liu TK, Song XM, Duan WK et al (2014) Genome-wide analysis and expression patterns of NAC transcription factor family under different developmental stages and abiotic stresses in Chinese cabbage. Plant Mol Biol Rep 32:1041–1056

    Article  Google Scholar 

  • Lu M, Ying S, Zhang DF et al (2012) A maize stress-responsive NAC transcription factor, ZmSNAC1, confers enhanced tolerance to dehydration in transgenic Arabidopsis. Plant Cell Rep 31:1701–1711

    Article  CAS  PubMed  Google Scholar 

  • Lu M, Zhang DF, Shi YS et al (2013) Expression of SbSNAC1, a NAC transcription factor from sorghum, confers drought tolerance to transgenic Arabidopsis. Plant Cell Tissue Organ Cult 115:443–455

    Article  CAS  Google Scholar 

  • Mao X, Zhang H, Qian X et al (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  PubMed Central  Google Scholar 

  • Mao XG, Chen SS, Li A et al (2014) Novel NAC transcription factor TaNAC67 confers enhanced multi-abiotic stress tolerances in Arabidopsis. PloS ONE 9:e84359

    Article  PubMed  PubMed Central  Google Scholar 

  • Mao HD, Qin F, Wang HW et al (2015) A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat Commun. doi:10.1038/ncomms9326

    Google Scholar 

  • Mao HD, Yu LJ, Han R et al (2016) ZmNAC55, a maize stress-responsive NAC transcription factor, confers drought resistance in transgenic Arabidopsis. Plant Physiol Biochem 105:55–66

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Movahedi A, Zhang JX, Yin TM et al (2015) Functional analysis of two orthologous NAC, genes, CarNAC3, and CarNAC6, from Cicer arietinum, involved in abiotic stresses in poplar. Plant Mol Biol Rep 33:1539–1551

    Article  CAS  Google Scholar 

  • Nuruzzaman M, Manimekalai R, Sharoni AM et al (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30–44

    Article  CAS  PubMed  Google Scholar 

  • Ooka H, Satoh K, Doi K et al (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247

    Article  CAS  PubMed  Google Scholar 

  • Oprea CA, Marin DI, Bolohan C (2015) Influence of some technological factors on grain sorghum (Sorghum bicolor (L.) Moench var. Eusorghum) yield grown under the conditions of Southeastern Romania. Agrolife Sci J 4:123–130

    Google Scholar 

  • Pascual MB, Cánovas FM, Ávila C et al (2015) The NAC transcription factor family in maritime pine (Pinus Pinaster): molecular regulation of two genes involved in stress responses. BMC Plant Biol 15:1–15

    Article  Google Scholar 

  • Rui QZ, Zheng HY (2015) The Arabidopsis NAC transcription factor NST2 functions together with SND1 and NST1 to regulate secondary wall biosynthesis in fibers of inflorescence stems. Plant Signal Behav 10:e989746

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Shahnejat-Bushehri S, Tarkowska D, Sakuraba Y et al (2016) Arabidopsis NAC transcription factor JUB1 regulates GA/BR metabolism and signaling. Nat Plants. doi:10.1038/nplants.2016.13

    PubMed  Google Scholar 

  • Shahnejat-Bushehri S, Allu AD, Mehterov N et al (2017) Arabidopsis NAC transcription factor JUNGBRUNNEN1 exerts conserved control over gibberellin and brassinosteroid metabolism and signaling genes in tomato. Front Plant Sci. doi:10.3389/fpls.2017.00214

    PubMed  PubMed Central  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  CAS  PubMed  Google Scholar 

  • Souer E, Van HA, Kloos D et al (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 HY, Zhang SZ, Yin YL et al (2015) Genome-wide analysis of NAM-ATAF1, 2-CUC2 transcription factor family in Solanum lycopersicum. J Plant Biochem Biotechnol 24:176–183

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F et al (1997) The CLUSTALX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nuclic Acids Res 25:4876–4882

    Article  CAS  Google Scholar 

  • Tran L, Nakashima K, Sakuma Y et al (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 

  • Wang N, Zheng Y, Xin HP et al (2013) Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep 32:61–75

    Article  PubMed  Google Scholar 

  • Wang ZY, Gehring C, Zhu J et al (2015) The Arabidopsis Vacuolar Sorting Receptor1 is required for osmotic stress-induced abscisic acid biosynthesis. Plant Physiol 167:137–152

    Article  CAS  PubMed  Google Scholar 

  • Xie Q, Guo HS, Dallman G et al (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419:167–170

    Article  CAS  PubMed  Google Scholar 

  • Xu ZY, Kim SY, Hyeon YD et al (2013) The Arabidopsis NAC transcription factor ANAC096 cooperates with bZIP-type transcription factors in dehydration and osmotic stress responses. Plant Cell 25:4708–4724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue GP, Bower NI, Mcintyre CL et al (2006) TaNAC69 from the 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

    Article  CAS  Google Scholar 

  • Xue GP, Way HM, Richardson T et al (2011) Overexpression of TaNAC69 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. Mol Plant 4:697–712

    Article  CAS  PubMed  Google Scholar 

  • Yang XW, Wang XY, Ji L et al (2015) Overexpression of a Miscanthus lutarioriparius NAC gene MlNAC5 confers enhanced drought and cold tolerance in Arabidopsis. Plant Cell Rep 34:943–958

    Article  CAS  PubMed  Google Scholar 

  • Yu XW, Liu YM, Wang S et al (2016) CarNAC4, a NAC-type chickpea transcription factor conferring enhanced drought and salt stress tolerances in Arabidopsis. Plant Cell Rep 35:1–15

    Article  Google Scholar 

  • Zhao X, Yang XW, Pei SQ et al (2016) The miscanthus NAC transcription factor MlNAC9 enhances abiotic stress tolerance in transgenic Arabidopsis. Gene 586:158–169

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The work was supported by National Natural Science Foundation of China (Grant No. 31501314), DaBeiNong young teachers’ Scientific Research Fund Project (Grant No. 1014115004/025), State Key laboratory of Crop Biology foundation (Grant No. 2015KF08) and the Scientific Research Project of Beijing Educational Committee (Grant No. KM201510020003).

Author information

Author notes

  1. Yibadaiti Kadier, Yi-yi Zu and Qing-min Dai have contributed to this work equally.

Authors and Affiliations

  1. College of Plant Science and Technology, Beijing University of Agriculture, Beijing, 102206, China

    Yibadaiti Kadier, Yi-yi Zu, Ge Song, Shi-wen Lin, Qing-peng Sun, Jin-bao Pan & Min Lu

  2. College of Ecology, Lishui University, Lishui, 323000, China

    Qing-min Dai

Authors
  1. Yibadaiti Kadier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yi-yi Zu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qing-min Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ge Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shi-wen Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qing-peng Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jin-bao Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Min Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Min Lu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 18 KB)

Supplementary material 2 (DOCX 197 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kadier, Y., Zu, Yy., Dai, Qm. et al. Genome-wide identification, classification and expression analysis of NAC family of genes in sorghum [Sorghum bicolor (L.) Moench]. Plant Growth Regul 83, 301–312 (2017). https://doi.org/10.1007/s10725-017-0295-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-017-0295-y

Keywords

Search

Navigation