Skip to main content

Ancient RNA

  • Chapter
  • First Online:
Book cover Paleogenomics

Part of the book series: Population Genomics ((POGE))

Abstract

Compared to other ancient biomolecules such as DNA and proteins, ancient RNA is arguably the least studied. The reasons behind this are largely based on a relative lack of surviving material due to RNA’s molecular properties. Increasingly powerful and sensitive molecular methods however now allow for trace amounts of ancient RNA to be sequenced, to previously unthinkable depths, and doing so has made available a previously untapped layer of -omic information. It is becoming possible to ascertain the activity of an ancient genome in vivo, and thus assess environmental stresses and pathogen interaction, and uncover further epigenomic mechanisms. In this chapter we will explore the past, present, and future applications of the new paleotranscriptomics.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
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

References

  • Allaby RG, et al. Using archaeogenomic and computational approaches to unravel the history of local adaptation in crops. Philos Trans R Soc Lond B Biol Sci. 2015;370(1660):20130377.

    Article  PubMed  PubMed Central  Google Scholar 

  • Awano N, Inouye M, Phadtare S. RNase activity of polynucleotide phosphorylase is critical at low temperature in Escherichia coli and is complemented by RNase II. J Bacteriol. 2008;190(17):5924–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bos KI, et al. Parallel detection of ancient pathogens via array-based DNA capture. Philos Trans R Soc Lond B Biol Sci. 2015;370(1660):20130375.

    Article  PubMed  PubMed Central  Google Scholar 

  • Briggs AW, et al. Patterns of damage in genomic DNA sequences from a Neandertal. Proc Natl Acad Sci U S A. 2007;104(37):14616–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Briggs AW, et al. Removal of deaminated cytosines and detection of in vivo methylation in ancient DNA. Nucleic Acids Res. 2010;38(6):e87.

    Article  PubMed  Google Scholar 

  • Brown TA, et al. Recent advances in ancient DNA research and their implications for archaeobotany. Veg Hist Archaeobotany. 2015;24(1):207–14.

    Article  Google Scholar 

  • Castello DJ, et al. Detection of tomato mosaic tobamovirus RNA in ancient glacial ice. Polar Biol. 1999;22(3):207–12.

    Article  Google Scholar 

  • Chomczynski P, Sacchi N. The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Protoc. 2006;1(2):581–5.

    Article  CAS  PubMed  Google Scholar 

  • Cooper A, Poinar HN. Ancient DNA: do it right or not at all. Science. 2000;289(5482):1139.

    Article  CAS  PubMed  Google Scholar 

  • Dabney J, et al. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc Natl Acad Sci. 2013;110(39):15758–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de los Rios A, Ramirez R, Estévez P. RNase in Lasallia hispanica and Cornicularia normoerica: multiplicity of electromorphs and activity changes during a hydration-dehydration cycle. J Exp Bot. 1996;47(12):1927–33.

    Article  Google Scholar 

  • Elbashir SM, Lendeckel W, Tuschl T. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev. 2001;15(2):188–200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evin A, et al. Unravelling the complexity of domestication: a case study using morphometrics and ancient DNA analyses of archaeological pigs from Romania. Philos Trans R Soc Lond B Biol Sci. 2015;370(1660):20130616.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fabre A-L, et al. An efficient method for long-term room temperature storage of RNA. Eur J Hum Genet. 2014;22(3):379–85.

    Article  CAS  PubMed  Google Scholar 

  • Fordyce SL, et al. Deep Sequencing of RNA from ancient maize kernels. PLoS One. 2013a;8(1):e50961.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fordyce SL, et al. Long-term RNA persistence in postmortem contexts. Investig Genet. 2013b;4(1):7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fraile A, et al. A century of tobamovirus evolution in an Australian population of Nicotiana glauca. J Virol. 1997;71(11):8316–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fu Q, et al. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature. 2014;514(7523):445–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ginolhac A, et al. mapDamage: testing for damage patterns in ancient DNA sequences. Bioinformatics. 2011;27(15):2153–5.

    Article  CAS  PubMed  Google Scholar 

  • Guy PL. Ancient RNA? RT-PCR of 50-year-old RNA identifies peach latent mosaic viroid. Arch Virol. 2013;158(3):691–4.

    Article  CAS  PubMed  Google Scholar 

  • Hanghøj K, et al. Fast, accurate and automatic ancient nucleosome and methylation maps with epiPALEOMIX. Mol Biol Evol. 2016;33:3284–98.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hansen AJ, et al. Crosslinks rather than strand breaks determine access to ancient DNA sequences from frozen sediments. Genetics. 2006;173(2):1175–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harris ME, Christian EL. RNA crosslinking methods. Methods Enzymol. 2009;468:127–46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higuchi R, et al. DNA sequences from the quagga, an extinct member of the horse family. Nature. 1984;312(5991):282–4.

    Article  CAS  PubMed  Google Scholar 

  • Hofreiter M, et al. DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA. Nucleic Acids Res. 2001;29(23):4793–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Y, Li L. DNA crosslinking damage and cancer – a tale of friend and foe. Transl Cancer Res. 2013;2(3):144–54.

    CAS  PubMed  Google Scholar 

  • Hussain S, et al. Characterizing 5-methylcytosine in the mammalian epitranscriptome. Genome Biol. 2013;14(11):215.

    Article  PubMed  PubMed Central  Google Scholar 

  • Huynen L, Millar CD, Lambert DM. Resurrecting ancient animal genomes: The extinct moa and more. BioEssays. 2012;34(8):661–9.

    Article  CAS  PubMed  Google Scholar 

  • Keller A, et al. miRNAs in ancient tissue specimens of the Tyrolean Iceman. Mol Biol Evol. 2017;34:793–801.

    CAS  PubMed  Google Scholar 

  • Kistler L, Ware R, Smith O, Collins MJ, Allaby RG. A new general model for ancient DNA decay based on paleogenomic meta-analysis. Nucleic Acids Res. 2017;45(11):6310–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laing LG, Draper DE. Thermodynamics of RNA folding in a conserved ribosomal RNA domain. J Mol Biol. 1994;237(5):560–76.

    Article  CAS  PubMed  Google Scholar 

  • Lindahl T. Irreversible heat inactivation of transfer ribonucleic acids. J Biol Chem. 1967;242(8):1970–3.

    CAS  PubMed  Google Scholar 

  • Meyer M, et al. A high-coverage genome sequence from an archaic Denisovan individual. Science. 2012;338(6104):222–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mouttham N, et al. Surveying the repair of ancient DNA from bones via high-throughput sequencing. BioTechniques. 2015;59(1):19.

    Article  CAS  PubMed  Google Scholar 

  • Müller R, Roberts CA, Brown TA. Biomolecular identification of ancient Mycobacterium tuberculosis complex DNA in human remains from Britain and continental Europe. Am J Phys Anthropol. 2014;153(2):178–89.

    Article  PubMed  Google Scholar 

  • Ng TFF, et al. Preservation of viral genomes in 700-y-old caribou feces from a subarctic ice patch. Proc Natl Acad Sci. 2014;111(47):16842–7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Orlando L, et al. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature. 2013;499(7456):74–8.

    Article  CAS  PubMed  Google Scholar 

  • Pääbo S. Molecular genetic investigations of ancient human remains. Cold Spring Harb Symp Quant Biol. 1986;51:441–6.

    Article  PubMed  Google Scholar 

  • Pääbo S. Ancient DNA: extraction, characterization, molecular cloning, and enzymatic amplification. Proc Natl Acad Sci U S A. 1989;86(6):1939–43.

    Article  PubMed  PubMed Central  Google Scholar 

  • Palmer SA, et al. Archaeogenomic evidence of punctuated genome evolution in Gossypium. Mol Biol Evol. 2012;29(8):2031–8.

    Article  CAS  PubMed  Google Scholar 

  • Paris HS. Overview of the origins and history of the five major cucurbit crops: issues for ancient DNA analysis of archaeological specimens. Veg Hist Archaeobotany. 2016;25:405–14.

    Article  Google Scholar 

  • Pinhasi R, et al. Optimal ancient DNA yields from the inner ear part of the human petrous bone. PLoS One. 2015;10(6):e0129102.

    Article  PubMed  PubMed Central  Google Scholar 

  • Poeckh T, et al. Adsorption and elution characteristics of nucleic acids on silica surfaces and their use in designing a miniaturized purification unit. Anal Biochem. 2008;373(2):253–62.

    Article  CAS  PubMed  Google Scholar 

  • Renaud G, et al. gargammel: a sequence simulator for ancient DNA. Bioinformatics. 2017;33:577–9.

    CAS  PubMed  Google Scholar 

  • Rogan PK, Salvo JJ. Study of nucleic acids isolated from ancient remains. Am J Phys Anthropol. 1990;33(S11):195–214.

    Article  Google Scholar 

  • Rogers SO, Bendich AJ. Ribosomal RNA genes in plants: variability in copy number and in the intergenic spacer. Plant Mol Biol. 1987;9(5):509–20.

    Article  CAS  PubMed  Google Scholar 

  • Rollo F. Characterisation by molecular hybridization of RNA fragments isolated from ancient (1400 B.C.) seeds. Theor Appl Genet. 1985;71(2):330–3.

    Article  CAS  PubMed  Google Scholar 

  • Rollo F, Venanzi FM, Amici A. Nucleic acids in mummified plant seeds: biochemistry and molecular genetics of pre-Columbian maize. Genet Res. 1991;58(3):193–201.

    Article  CAS  PubMed  Google Scholar 

  • Rollo F, Venanzi FM, Amici A. DNA and RNA from ancient plant seeds. In: Herrmann B, Hummel S, editors. Ancient DNA: recovery and analysis of genetic material from paleontological, archaeological, museum, medical, and forensic specimens. New York: Springer; 1994. p. 218–36.

    Chapter  Google Scholar 

  • Sallon S, et al. Germination, genetics, and growth of an ancient date seed. Science. 2008;320(5882):1464.

    Article  CAS  PubMed  Google Scholar 

  • Schaefer M, et al. RNA cytosine methylation analysis by bisulfite sequencing. Nucleic Acids Res. 2009;37(2):e12.

    Article  PubMed  Google Scholar 

  • Schuenemann VJ, et al. Targeted enrichment of ancient pathogens yielding the pPCP1 plasmid of Yersinia pestis from victims of the Black Death. Proc Natl Acad Sci. 2011;108(38):E746–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seguin-Orlando A, et al. Paleogenomics. Genomic structure in Europeans dating back at least 36,200 years. Science. 2014;346(6213):1113–8.

    Article  CAS  PubMed  Google Scholar 

  • Skoglund P, et al. Ancient wolf genome reveals an early divergence of domestic dog ancestors and admixture into high-latitude breeds. Curr Biol. 2015;25(11):1515–9.

    Article  CAS  PubMed  Google Scholar 

  • Smith O. Small RNA-mediated regulation, adaptation and stress response in barley archaeogenome. PhD thesis, School of Life Sciences, University of Warwick; 2012.

    Google Scholar 

  • Smith O, et al. A complete ancient RNA genome: identification, reconstruction and evolutionary history of archaeological Barley Stripe Mosaic Virus. Sci Rep. 2014a;4:4003.

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith O, et al. Genomic methylation patterns in archaeological barley show de-methylation as a time-dependent diagenetic process. Sci Rep. 2014b;4:5559.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith O, et al. Sedimentary DNA from a submerged site reveals wheat in the British Isles 8000 years ago. Science. 2015;347(6225):998–1001.

    Article  CAS  PubMed  Google Scholar 

  • Smith O, et al. Small RNA activity in archaeological barley shows novel germination inhibition in response to environment. Mol Biol Evol. 2017;34(10):2555–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snead NM, Rossi JJ. Biogenesis and function of endogenous and exogenous siRNAs. Wiley Interdiscip Rev RNA. 2010;1(1):117–31.

    Article  CAS  PubMed  Google Scholar 

  • Spanò C, Buselli R, Grilli I. Dormancy and germination in wheat embryos: ribonucleases and hormonal control. Biol Plant. 2008;52(4):660.

    Article  Google Scholar 

  • Squires JE, et al. Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic Acids Res. 2012;40(11):5023–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stahl EA, Bishop JG. Plant-pathogen arms races at the molecular level. Curr Opin Plant Biol. 2000;3(4):299–304.

    Article  CAS  PubMed  Google Scholar 

  • Sutton DH, Brown T. The dependence of DNase I activity on the conformation of oligodeoxynucleotides. Biochem J. 1997;321(2):481–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuschl T, et al. Modified RNA ligase for efficient 3′ modification of RNA. Google Patents; 2014.

    Google Scholar 

  • Venanzi FM, Rollo F. Mummy RNA lasts longer. Nature. 1990;343(6253):25–6.

    Article  CAS  PubMed  Google Scholar 

  • Vernot B, Akey JM. Complex history of admixture between modern humans and Neandertals. Am J Hum Genet. 2015;96(3):448–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willerslev E, Cooper A. Review paper. Ancient DNA. Proc R Soc B Biol Sci. 2005;272(1558):3–16.

    Article  CAS  Google Scholar 

  • Willerslev E, Hansen AJ, Poinar HN. Isolation of nucleic acids and cultures from fossil ice and permafrost. Trends Ecol Evol. 2004;19(3):141–7.

    Article  PubMed  Google Scholar 

  • Winter J, et al. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol. 2009;11(3):228–34.

    Article  CAS  PubMed  Google Scholar 

  • Worobey M. Phylogenetic evidence against evolutionary stasis and natural abiotic reservoirs of influenza A virus. J Virol. 2008;82(7):3769–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yashina S, et al. Regeneration of whole fertile plants from 30,000-y-old fruit tissue buried in Siberian permafrost. Proc Natl Acad Sci U S A. 2012;109(10):4008–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang G, et al. Evidence of influenza A virus RNA in Siberian lake ice. J Virol. 2006;80(24):12229–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zuker M, Mathews DH, Turner DH. Algorithms and thermodynamics for RNA secondary structure prediction: a practical guide. In: Barciszewski J, Clark BFC, editors. RNA biochemistry and biotechnology. Dordrecht: Springer; 1999. p. 11–43.

    Chapter  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Oliver Smith .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Smith, O., Gilbert, M.T.P. (2018). Ancient RNA. In: Lindqvist, C., Rajora, O. (eds) Paleogenomics. Population Genomics. Springer, Cham. https://doi.org/10.1007/13836_2018_17

Download citation

Publish with us

Policies and ethics