Skip to main content
SpringerLink
Log in

NGS-Based Expression Profiling of HSP Genes During Cold and Freeze Stress in Seabuckthorn (Hippophae rhamnoides L.)

  • Chapter
  • First Online:
Heat Shock Proteins and Plants

Part of the book series: Heat Shock Proteins ((HESP,volume 10))

Abstract

Expression of many Heat Shock Protein (HSP) genes triggers in plant cells when exposed to abiotic stresses. An important exercise towards understanding the mechanism of plants response to cold and freeze stress is the identification of genes responsible for cold and freeze tolerance in plants adapted to low temperature climates. Seabuckthorn (Hippophae rhamnoides L.) is one such plant species that sustains growth in extreme temperature environments. We performed complete transcriptome profiling of leaf and root tissues of seabuckthorn using Illumina Next Generation Sequencing. The seabuckthorn transcriptome data revealed the presence of 205 heat shock protein and their co-protein coding genes. Later, DeepSAGE, a tag based approach, was used to identify differentially expressed genes coding for HSPs and their co-proteins under cold and freeze stress. The DeepSAGE data revealed differential expression of 13 genes under cold stress (CS) and 9 genes under freeze stress (FS) with respect to control (CON). Similarly, 14 genes were differentially expressed under FS with respect to CS. Expression of the most abundant hsp70 gene was validated using qRT-PCR under different stress treatments. Our results may assist future efforts aiming towards understanding the role of HSP genes in mediating cold and freeze stress in crop plants.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ABA:

abscisic acid

CA:

cold acclimation

CTAB:

cetyl trimethylammonium bromide

DeepSAGE:

deep serial analysis of gene expression

DEGs:

differentially expressed genes

ER:

endoplasmic reticulum

EST:

expressed sequence tag

FDR:

false discovery rate

GEO:

gene expression omnibus

GO:

gene ontology

GPAT:

glycerol-3-phosphate acyltransferase

HSF:

heat shock factor

HSP:

heat shock protein

hsp :

heat shock protein gene

KEGG:

Kyoto encyclopedia of genes and genomes

LT:

low temperature

MPSS:

massive parallel signature sequencing

NGS:

next generation sequencing

RIN:

RNA integrity number

SAGE:

serial analysis of gene expression

SRA:

short read archive

SSR:

simple sequence repeats

References

  • Akkermans ADL, Roelofsen W, Blom J, Hussdanell K, Harkink R (1983) Utilization of carbon and nitrogen compounds by Frankia in synthetic media and in root nodules of Alnus glutinosa, Hippophae rhamnoides, and Datisca cannabina. Can J Bot 61:2793–2800

    Article  CAS  Google Scholar 

  • Ansorge WJ (2009) Next-generation DNA sequencing techniques. New Biotechnol 25:195–203

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bae MS, Cho EJ, Choi EY, Park OK (2003) Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J 36:652–663

    Article  CAS  PubMed  Google Scholar 

  • Bartish IV, Jeppsson N, Nybom H, Swenson U (2002) Phylogeny of Hippophae (Elaeagnaceae) inferred from parsimony analysis of chloroplast DNA and morphology. Syst Bot 27:41–54

    Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. In: Post-transcriptional control of gene expression in plants. Springer, Dordrecht, pp 191–222

    Chapter  Google Scholar 

  • Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D, Luo S, McCurdy S, Foy M, Ewan M, Roth R (2000) Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat Biotechnol 18:630–634

    Article  CAS  PubMed  Google Scholar 

  • Chaudhary S, Sharma PC (2015) DeepSAGE based differential gene expression analysis under cold and freeze stress in seabuckthorn (Hippophae rhamnoides L.). PLoS One 10:e0121982

    Article  PubMed  PubMed Central  Google Scholar 

  • Chawla A, Stobdan T, Srivastava RB, Jaiswal V, Chauhan RS, Kant A (2015) Sex-based temporal gene expression in male and female floral buds of seabuckthorn (Hippophae rhamnoides). PLoS One 10:e0124890

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng MY, Hartl FU, Martin J, Pollock RA, Kalousek F, Neupert W, Hallberg EM, Hallberg RL, Horwich A (1989) Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 6208:585–674

    Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126:52–61

    Article  CAS  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  CAS  PubMed  Google Scholar 

  • Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  • Elena T, Capraru G, Rosu CM, Zamfirache MM, Olteanu Z, Manzu C (2011) Morphometric pattern of somatic chromosomes in three Romanian seabuckthorn genotypes. Caryologia 64:189–196

    Article  Google Scholar 

  • Fatima T, Snydrez CL, Schoeder WR, Cram D, Datla R, Wishat D, Krishna P (2012) Fatty acid composition of developing Seabuckthorn (Hippophae rhamnoides L.) berry and transcriptome of the mature seeds. PLoS One 7:e34099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghangal R, Raghuvanshi S, Sharma PC (2009) Isolation of good quality RNA from a medicinal plant seabuckthorn, rich in secondary metabolites. Plant Physiol Biochem 47:1113–1115

    Article  CAS  PubMed  Google Scholar 

  • Ghangal R, Raghuvanshi S, Sharma PC (2012) Expressed sequence tag based identification and expression analysis of some cold inducible elements in seabuckthorn (Hippophae rhamnoides L.). Plant Physiol Biochem 51:123–128

    Article  CAS  PubMed  Google Scholar 

  • Ghangal R, Chaudhary S, Jain M, Purty RS, Sharma PC (2013) Optimization of de novo short read assembly of seabuckthorn (Hippophae rhamnoides L.) transcriptome. PLoS One 8:e72516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 26:644–652

    Article  Google Scholar 

  • Gupta R, Deswal R (2012) Low temperature stress modulated secretome analysis and purification of antifreeze protein from Hippophae rhamnoides, a Himalayan wonder plant. J Proteome Res 11:2684–2696

    Article  CAS  PubMed  Google Scholar 

  • Gupta SM, Ahmed Z, Kumar N (2009) Isolation of cDNA fragment of glycerol-3-phosphate acyltransferase gene from seabuckthorn. Def Sci J 59:147–151

    Article  CAS  Google Scholar 

  • Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol 142:98–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jain M (2011) Next-generation sequencing technologies for gene expression profiling in plants. Brief Funct Genomics 11:63–70

    Article  PubMed  Google Scholar 

  • Jain A, Ghangal R, Grover A, Raghuvanshi S, Sharma PC (2010) Development of EST-based new SSR markers in seabuckthorn. Physiol Mol Biol Plants 16:375–378

    Article  PubMed  PubMed Central  Google Scholar 

  • Jain A, Chaudhary S, Sharma PC (2014) Mining of microsatellites using next generation sequencing of seabuckthorn (Hippophae rhamnoides L.) transcriptome. Physiol Mol Biol Plants 20:115–123

    Article  CAS  PubMed  Google Scholar 

  • Kadota Y, Shirasu K (2012) The HSP90 complex of plants. Biochim Biophys Acta 1823:689–697

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484

    Article  CAS  PubMed  Google Scholar 

  • Kawamura Y, Uemura M (2003) Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J 36:141–154

    Article  CAS  PubMed  Google Scholar 

  • Ledwood JS, Shimwell DW (1971) Growth rates of Hippophae rhamnoides L. Ann Bot 35:1053–1058

    Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stress, vol 1: chilling, freezing, and high temperature stress. Academic, New York

    Google Scholar 

  • Li Z, Srivastava P (2004) Heat‐shock proteins. Curr Protoc Immunol A-1T

    Google Scholar 

  • Li C, Yang Y, Junttila O, Palva ET (2005) Sexual differences in cold acclimiation and freezing tolerance development in sea buckthorn (Hippophae rhamnoides L.) ecotypes. Plant Sci 168:1365–1370

    Article  CAS  Google Scholar 

  • Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, Li S (2009) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272

    Article  PubMed  Google Scholar 

  • Lian YS, Chen XL (2000) The regular patterns of distribution on the natural components in plants of the genus Hippophae L. J Northwest Normal Univ (Nat Sci Ed) 36:113–128

    CAS  Google Scholar 

  • Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631–677

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Matas MA, Nuñez P, Soto A, Allona I, Casado R, Collada C, Guevara MA, Aragoncillo C, Gomez L (2004) Protein cryoprotective activity of a cytosolic small heat shock protein that accumulates constitutively in chestnut stems and is up-regulated by low and high temperatures. Plant Physiol 134:1708–1717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu R (1992) Seabuckthorn – a multipurpose plant for fragile mountains, International Centre for Integrated Mountain Development (ICIMOD) occasional paper no. 20. International Centre for Integrated Mountain Development, Kathmandu

    Google Scholar 

  • Lu R (1997) Eco-geographical distribution of seabuckthorn and prospects of international cooperation. In: Worldwide research & development of seabuckthorn. Science Publishing House & Technology Press, Beijing, pp 11–22

    Google Scholar 

  • Mayer M, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morozova O, Hirst M, Marra MA (2009) Application of new sequencing technologies for transcriptome analysis. Annu Rev Genomics Hum Genet 10:135–151

    Article  CAS  PubMed  Google Scholar 

  • Morrissy S, Morin RD, Delaney A, Zeng T, McDonald H, Jones S, Zhao Y, Hirst M, Marra MA (2009) Next-generation tag sequencing for cancer gene expression profiling. Genome Res 19:1825–1835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nielsen KL, Hogh AL, Emmersen J (2006) DeepSAGE—digital transcriptomics with high sensitivity, simple experimental protocol and multiplexing of samples. Nucleic Acids Res 34:e133

    Article  PubMed  PubMed Central  Google Scholar 

  • Ozsolak F, Milos PM (2011) RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 12:87–98

    Article  CAS  PubMed  Google Scholar 

  • Patel RK, Jain M (2012) NGS QC toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 7:e30619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Renaut J, Lutts S, Hoffmann L, Hausman JF (2004) Responses of poplar to chilling temperatures: proteomic and physiological aspects. Plant Biol 6:81–90

    Article  CAS  PubMed  Google Scholar 

  • Santoro MG (2000) Heat shock factors and the control of the stress response. Biochem Pharmacol 59:55–63

    Article  CAS  PubMed  Google Scholar 

  • Schlesinger MJ (1990) Heat shock proteins. J Biol Chem 265:12111–12114

    CAS  PubMed  Google Scholar 

  • Schulz MH, Zerbino DR, Vingron M, Birney E (2012) Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28:1086–1092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schuster SC (2008) Next-generation sequencing transforms today’s biology. Nat Methods 5:16–18

    Article  CAS  PubMed  Google Scholar 

  • Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19:1117–1123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stobdan T, Angchuk D, Singh SB (2008) Seabuckthorn: an emerging storehouse for researchers in India. Curr Sci 94:1236–1237

    Google Scholar 

  • Suryakumar G, Gupta A (2011) Medicinal and therapeutic potential of Seabuckthorn (Hippophae rhamnoides L.). J Ethnopharmacol 138:268–278

    Google Scholar 

  • t’Hoen PA, Ariyurek Y, Thygesen HH, Vreugdenhil E, Vossen RH, deMenezes RX, Boer JM, van Ommen GJB, den Dunnen JT (2008) Deep sequencing based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res 36:e141

    Article  Google Scholar 

  • Taylor NL, Heazlewood JL, Day DA, Millar AH (2005) Differential impact of environmental stresses on the pea mitochondrial proteome. Mol Cell Proteomics 4:1122–1133

    Article  CAS  PubMed  Google Scholar 

  • Teng BS, Lu YH, Wang ZT, Tao XY, Wei DZ (2006) In vitro anti-tumor activity of isorhamnetin isolated from Hippophae rhamnoides L. against BEL-7402 cells. Pharmacol Res 54:186–194

    Article  CAS  PubMed  Google Scholar 

  • Thakur V, Varshney R (2010) Challenges and strategies for next generation sequencing (NGS) data analysis. J Comput Sci Syst Biol 3:040–042

    Article  Google Scholar 

  • Trajkovsk V, Jeppsson N (1999) Domestication of seabuckthorn. Bot Lith 2:37–46

    Google Scholar 

  • Unamba CIN, Nag A, Sharma RK (2015) Next generation sequencing technologies: the doorway to the unexplored genomics of non-model plants. Front Plant Sci 6:1074

    Article  PubMed  PubMed Central  Google Scholar 

  • Velculescu VE, Zhang L, Vogelstein B, Kinzler KW (1995) Serial analysis of gene expression. Science 270:484–487

    Article  CAS  PubMed  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Yao Y, Xu G, Li C (2005) Growth and physiological responses to drought and elevated ultraviolet‐B in two contrasting populations of Hippophae rhamnoides. Physiol Plant 124:431–440

    Article  CAS  Google Scholar 

  • Zeb A (2006) Anticarcinogenic potential of lipids from Hippophae; Evidence from the recent literature. Asian Pac J Cancer Prev 7:32–35

    PubMed  Google Scholar 

  • Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the financial support provided by the Department of Biotechnology, Government of India.

Author information

Authors and Affiliations

  1. University School of Biotechnology, Guru Gobind Singh Indraprastha University, New Delhi, India

    P. C. Sharma & Saurabh Chaudhary

Authors
  1. P. C. Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saurabh Chaudhary
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. C. Sharma .

Editor information

Editors and Affiliations

  1. Department of Neuroscience, University of Dammam, Damman, Saudi Arabia

    Alexzander A. A. Asea

  2. Division of Molecular and Cellular Biology Department of Radiation Oncology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts, USA

    Punit Kaur

  3. Department of Radiation Oncology, University of Texas MD Anderson Cancer Center, Houston, Texas, USA

    Stuart K. Calderwood

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Sharma, P.C., Chaudhary, S. (2016). NGS-Based Expression Profiling of HSP Genes During Cold and Freeze Stress in Seabuckthorn (Hippophae rhamnoides L.). In: Asea, A., Kaur, P., Calderwood, S. (eds) Heat Shock Proteins and Plants. Heat Shock Proteins, vol 10. Springer, Cham. https://doi.org/10.1007/978-3-319-46340-7_15

Download citation

Publish with us

Policies and ethics

Search

Navigation