Skip to main content
SpringerLink
Log in

Comprehensive transcriptional profiling of NaHCO3-stressed Tamarix hispida roots reveals networks of responsive genes

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Root tissue is the primary site of perception for stress from soil, and is the main tissue involved in stress response. Tamarix hispida is a woody halophyte that is highly tolerant to salt and drought stress, but little information available about gene expression in roots in response to abiotic stress. In this study, eight transcriptomes from roots of T. hispida treated with NaHCO3 for 0, 12, 24 and 48 h (two biological replicates were set at each time point) were built. In total, 47,324 unigenes were generated, and 6,267 differentially expressed genes (DEGs) were identified. There were 2,510, 3,690, and 2,636 genes significantly differentially expressed after stress for 12, 24 and 48 h, respectively. Co-expressed DEGs were clustered into ten classes (P < 0.001). Gene ontology enrichment analysis showed that 13 pathways were highly enriched, such as signal transduction, cell wall, phosphatase activity, and lipid kinase activity, suggesting that these pathways play important roles in the saline–alkaline response. Furthermore, the genes involved in lignin metabolic processes and biosynthesis of proline and trehalose are found closely involved in NaHCO3 stress response. This systematic analysis may provide an in-depth view of stress tolerance mechanisms in T. hispida.

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

Similar content being viewed by others

Abbreviations

CTAB:

Hexadecyltrimethylammonium bromide

DEGs:

Differentially expressed genes

DGE:

Digital gene expression

FDR:

False discovery rate

GO:

Gene ontology

NGS:

Next-generation sequencing

RPKM:

Reads per kilobase of exon model per million mapped reads

RT-PCR:

Reverse transcripion-PCR

TUGs:

Tentative unigenes

References

  • Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7(10):986–995

    PubMed  CAS  Google Scholar 

  • Boucher V, Buitink J, Lin X, Boudet J, Hoekstra FA, Hundertmark M, Renard D, Leprince O (2010) MtPM25 is an atypical hydrophobic late embryogenesis-abundant protein that dissociates cold and desiccation-aggregated proteins. Plant, Cell Environ 33(3):418–430

    Article  CAS  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11(2):113–116

    Article  CAS  Google Scholar 

  • Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676

    Article  PubMed  CAS  Google Scholar 

  • Crowe JH (2008) Trehalose and anhydrobiosis: the early work of JS Clegg. J Exp Biol 211(18):2899–2900

    Article  PubMed  Google Scholar 

  • Cuddapah S, Barski A, Cui K, Schones DE, Wang Z, Wei G, Zhao K (2009) Native chromatin preparation and Illumina/Solexa library construction. Cold Spring Harb Protoc 2009(6):pdb-prot5237

  • Dauwe R, Morreel K, Goeminne G, Gielen B, Rohde A, Van Beeumen J, Ralph J, Boudet A-M, Kopka J, Rochange SF (2007) Molecular phenotyping of lignin-modified tobacco reveals associated changes in cell-wall metabolism, primary metabolism, stress metabolism and photorespiration. Plant J 52(2):263–285

    Article  PubMed  CAS  Google Scholar 

  • Ernst J, Bar-Joseph Z (2006) STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics 7(1):191

    Article  PubMed  Google Scholar 

  • Ge Y, Li Y, Zhu YM, Bai X, Lv DK, Guo DJ, Ji W, Cai H (2010) Global transcriptome profiling of wild soybean (Glycine soja) roots under NaHCO3 treatment. BMC Plant Biol 10(1):153

    Article  PubMed  Google Scholar 

  • Ge Y, Li Y, Lv DK, Bai X, Ji W, Cai H, Wang AX, Zhu YM (2011) Alkaline-stress response in Glycine soja leaf identifies specific transcription factors and ABA-mediated signaling factors. Funct Integr Genomics 11(2):369–379

    Article  PubMed  CAS  Google Scholar 

  • Hara M, Shinoda Y, Tanaka Y, Kuboi T (2009) DNA binding of citrus dehydrin promoted by zinc ion. Plant, Cell Environ 32(5):532–541

    Article  CAS  Google Scholar 

  • Hegedűs Z, Zakrzewska A, Ágoston VC, Ordas A, Rácz P, Mink M, Spaink HP, Meijer AH (2009) Deep sequencing of the zebrafish transcriptome response to mycobacterium infection. Mol Immunol 46(15):2918–2930

    Article  PubMed  Google Scholar 

  • Hu YL, Gai Y, Yin L, Wang XX, Feng CY, Feng L, Li DF, Jiang XN, Wang DC (2010) Crystal structures of a Populus tomentosa 4-coumarate: CoA ligase shed light on its enzymatic mechanisms. Plant Cell 22(9):3093–3104

    Article  PubMed  CAS  Google Scholar 

  • Hwang EW, Kim KA, Park SC, Jeong MJ, Byun MO, Kwon HB (2005) Expression profiles of hot pepper (Capsicum annuum) genes under cold stress conditions. J Biosci 30(5):657–667

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6(1):25

    Article  PubMed  Google Scholar 

  • Jiang C, Xu J, Zhang H, Zhang X, Shi J, Li M, Ming F (2009) A cytosolic class I small heat shock protein, RcHSP17. 8, of Rosa chinensis confers resistance to a variety of stresses to Escherichia coli, yeast and Arabidopsis thaliana. Plant, Cell Environ 32(8):1046–1059

    Article  CAS  Google Scholar 

  • Karsi A, Cao D, Li P, Patterson A, Kocabas A, Feng J, Ju Z, Mickett KD, Liu Z (2002) Transcriptome analysis of channel catfish (Ictalurus punctatus): initial analysis of gene expression and microsatellite-containing cDNAs in the skin. Gene 285(1):157–168

    Article  PubMed  CAS  Google Scholar 

  • Kaye C, Neven L, Hofig A, Li QB, Haskell D, Guy C (1998) Characterization of a gene for spinach CAP160 and expression of two spinach cold-acclimation proteins in tobacco. Plant Physiol 116(4):1367–1377

    Article  PubMed  CAS  Google Scholar 

  • Kovacs D, Kalmar E, Torok Z, Tompa P (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol 147(1):381–390

    Article  PubMed  CAS  Google Scholar 

  • Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20(2):265–272

    Article  PubMed  CAS  Google Scholar 

  • Li HW, Zang BS, Deng XW, Wang XP (2011) Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234(5):1007–1018

    Article  PubMed  CAS  Google Scholar 

  • Libault M, Farmer A, Joshi T, Takahashi K, Langley RJ, Franklin LD, He J, Xu D, May G, Stacey G (2010) An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants. Plant J 63(1):86–99

    PubMed  CAS  Google Scholar 

  • Luyckx J, Baudouin C (2011) Trehalose: an intriguing disaccharide with potential for medical application in ophthalmology. Clinical Ophthalmology (Auckland, NZ) 5:577

    CAS  Google Scholar 

  • Maqbool A, Abbas W, Rao AQ, Irfan M, Zahur M, Bakhsh A, Riazuddin S, Husnain T (2010) Gossypium arboreum GHSP26 enhances drought tolerance in Gossypium hirsutum. Biotechnol Prog 26(1):21–25

    PubMed  CAS  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621–628

    Article  PubMed  CAS  Google Scholar 

  • Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B (2003) TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19(5):651–652

    Article  PubMed  CAS  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30(9):e36

    Article  PubMed  Google Scholar 

  • Qing DJ, Lu HF, Li N, Dong HT, Dong DF, Li YZ (2009) Comparative profiles of gene expression in leaves and roots of maize seedlings under conditions of salt stress and the removal of salt stress. Plant Cell Physiol 50(4):889–903

    Article  PubMed  CAS  Google Scholar 

  • Rampino P, Pataleo S, Gerardi C, Mita G, Perrotta C (2006) Drought stress response in wheat: physiological and molecular analysis of resistant and sensitive genotypes. Plant, Cell Environ 29(12):2143–2152

    Article  CAS  Google Scholar 

  • Sharma S, Verslues P (2010) Mechanisms independent of abscisic acid (ABA) or proline feedback have a predominant role in transcriptional regulation of proline metabolism during low water potential and stress recovery. Plant, Cell Environ 33(11):1838–1851

    Article  CAS  Google Scholar 

  • Sun Y, Wang F, Wang N, Dong Y, Liu Q, Zhao L, Chen H, Liu W, Yin H, Zhang X (2013) Transcriptome exploration in Leymus chinensis under saline–alkaline treatment using 454 pyrosequencing. PLoS ONE 8(1):e53632

    Article  PubMed  CAS  Google Scholar 

  • Teramoto N, Sachinvala ND, Shibata M (2008) Trehalose and trehalose-based polymers for environmentally benign, biocompatible and bioactive materials. Molecules 13(8):1773–1816

    Article  PubMed  CAS  Google Scholar 

  • Verdoy D, Coba de la Peña T, Redondo F, Lucas MM, Pueyo JJ (2006) Transgenic Medicago truncatula plants that accumulate proline display nitrogen-fixing activity with enhanced tolerance to osmotic stress. Plant, Cell Environ 29(10):1913–1923

    Article  CAS  Google Scholar 

  • Vorob’eva L, Pankova E (2008) Saline–alkali soils of Russia. Eurasian Soil Science 41(5):457–470

    Article  Google Scholar 

  • Wall PK, Leebens-Mack J, Chanderbali A, Barakat A, Wolcott E, Liang H, Landherr L, Tomsho L, Hu Y, Carlson J (2009) Comparison of next generation sequencing technologies for transcriptome characterization. BMC Genomics 10(1):347

    Article  PubMed  Google Scholar 

  • Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34(suppl 2):W293–W297

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Takano T, Liu S (2006) Identification of a mitochondrial ATP synthase small subunit gene (RMtATP6) expressed in response to salts and osmotic stresses in rice (Oryza sativa L.). J Exp Bot 57(1):193–200

    Article  PubMed  CAS  Google Scholar 

  • Zhou X, Su Z, Sammons RD, Peng Y, Tranel P, Stewart CN, Yuan J (2009) Novel software package for cross-platform transcriptome analysis (CPTRA). BMC Bioinformatics 10(Suppl 11):S16

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Foundation for the Author of National Excellent Doctoral Dissertation of China (200973) and Funds for Distinguished Young Scientists of Heilongjiang Province (Grant No. JC201102). We thank the editor and reviewers for their critical comments and thoughtful suggestions.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, 26 Hexing Road, Harbin, 150040, China

    Chao Wang, Caiqiu Gao, Liuqiang Wang, Lei Zheng, Chuanping Yang & Yucheng Wang

Authors
  1. Chao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Caiqiu Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liuqiang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lei Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chuanping Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yucheng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Chuanping Yang or Yucheng Wang.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, C., Gao, C., Wang, L. et al. Comprehensive transcriptional profiling of NaHCO3-stressed Tamarix hispida roots reveals networks of responsive genes. Plant Mol Biol 84, 145–157 (2014). https://doi.org/10.1007/s11103-013-0124-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-013-0124-2

Keywords

Search

Navigation