Paleogenomics pp 205-224 | Cite as

Herbarium Genomics: Plant Archival DNA Explored

  • Freek T. BakkerEmail author
Part of the Population Genomics book series (POGE)


Herbarium genomics, allowing testing of historic biological hypotheses in plant science, is a promising field mainly driven by recent advances in next-generation sequencing (NGS) technology. Herbarium collections represent an enormous botanical repository of both specimens and of phenotypic observations and locality data, of sometimes long-extinct taxa. Herbarium specimens, a large part of which stem from the nineteenth and eighteenth century, are mostly pressed and mounted and were usually heat-treated and poisoned for preservation. Whereas the presence of post-mortem damage in herbarium DNA has been found to consist of mainly genome fragmentation (single- and double-stranded breaks), damage-derived miscoding lesions appear to be highly limited or even negligible. For organelle genomes and other repetitive genomic compartments, genome skimming appears effective in retrieving sequence data from plant herbarium specimens, whereas studies addressing herbarium nuclear-encoded genes and particularly whole genomes are still in minority. High levels of herbarium genomic fragmentation possibly lead to insert sizes being smaller than Illumina read lengths applied. Using a series of 93 herbarium DNA samples, representing 10 angiosperm families, near-complete plastomes were assembled for 80% of the specimens, some of which are 146 years old. Overlapping read pairs were found to occur in roughly 80% of all read pairs obtained. After merging such overlapping pairs, the resulting fragments and their distribution can be considered to reflect the ongoing process of genome fragmentation up to the moment of DNA extraction. Fragment length distributions appear to fit gamma distributions with either many small fragments present or an increasing number of longer fragments having accumulated. These distributions appear to differ from usually observed first-order genomic degradation kinetics, possibly due to the nonrepresentative nature of genome skimming samples.


Genomic fragmentation Herbarium DNA Plant aDNA Plastomics 


  1. Allentoft ME, Collins M, Harker D, Haile J, Oskam CL, Hale ML, Campos PF, Samaniego JA, Gilbert MTP, Willerslev E, Zhang G, Scofield RP, Holdaway RN, Michael B. The half-life of DNA in bone: measuring decay kinetics in 158 dated fossils. Proc R Soc B. 2012;279(1748):4724–33. Epub 2012 Oct 10.CrossRefPubMedGoogle Scholar
  2. Ardui S, Ameur A, Vermeesch JR, Hestand MS. Single molecule real-time (SMRT) sequencing comes of age: applications and utilities for medical diagnostics. Nucleic Acids Res. 2018;46:2159–68. Scholar
  3. Bakker FT. DNA sequences from plant herbarium tissue. In: Hörandl E, Appelhans M, editors. Next-generation sequencing in plant systematics. Bratislava: International Association for Plant Taxonomy (IAPT); 2015. p. 271–84.Google Scholar
  4. Bakker FT. Herbarium genomics: skimming and plastomics from archival specimens. Webbia. 2017;72:35. Scholar
  5. Bakker FT, Lei D, Yu J, Mohammadin S, Wei Z, Van de Kerke S, Gravendeel B, Nieuwenhuis M, Staats M, Alquezar-Planas DE, Holmer R. Herbarium genomics: plastome sequence assembly from a range of herbarium specimens using an iterative organelle genome assembly (IOGA) pipeline. Biol J Linn Soc. 2016;117:3343. Scholar
  6. Bebber DP, Carine MA, Wood JRI, Wortley AH, Harris DJ, Prance GT, Davidse G, Paige J, Pennington TD, Robson NKB, Scotland RW. Herbaria are a major frontier for species discovery. PNAS. 2010;107:2216971.CrossRefGoogle Scholar
  7. Beck JB, Semple JC. Next-generation sampling: pairing genomics with herbarium specimens provides species-level signal in Solidago (Asteraceae). Appl Plant Sci. 2015;3(6):1500014. Scholar
  8. Besnard G, Christin P-A, Malé P-JG, L’huillier E, Lauzeral C, Coissac E, Vorontsova MS. From museums to genomics: old herbarium specimens shed light on a C3 to C4 transition. J Exp Bot. 2014;65:6711. Scholar
  9. Bieker VC, Martin MD. Implications and future prospects for evolutionary analyses of DNA in historical herbarium collections. Bot Lett. 2018; Scholar
  10. Bressan EA, Rossi ML, Gerald LT, Figueira A. Extraction of high-quality DNA from ethanol-preserved tropical plant tissues. BMC Res Notes. 2014;7:268. Scholar
  11. Briggs AW, Stenzel U, Johnson PLF, Green RE, Kelso J, Prufer K, Meyer M, Krause J, Ronan MT, Lachmann M, Pääbo S. Patterns of damage in genomic DNA sequences from a Neandertal. PNAS. 2007;104:14616–21. Scholar
  12. Brotherton P, Endicott P, Sanchez JJ, Beaumont M, Barnett R, Austin J, Cooper A. Novel high-resolution characterization of ancient DNA reveals C > U-type base modification events as the sole cause of post mortem miscoding lesions. Nucleic Acids Res. 2007;35(17):5717–28. Scholar
  13. Buerki S, Baker WJ. Collections-based research in the genomic era. Biol J Linn Soc. 2015;117:5. Scholar
  14. Chomicki G, Renner SS. Watermelon origin solved with molecular phylogenetics including Linnaean material: another example of museomics. New Phytol. 2015;205:526–32.CrossRefGoogle Scholar
  15. Clark SC, Egan R, Frazier PI, Wang Z. ALE: a generic assembly likelihood evaluation framework for assessing the accuracy of genome and metagenome assemblies. Bioinformatics. 2013;29:435–43.CrossRefGoogle Scholar
  16. Costion CM, Lowe AJ, Rossetto M, Kooyman RM, Breed MF, Ford A, Crayn DM. Building a plant DNA barcode reference library for a diverse tropical flora: an example from Queensland, Australia. Divers Distrib. 2016;8:1–9. Scholar
  17. Délye C, Deulvot C, Chauvel B. DNA analysis of herbarium specimens of the grass weed Alopecurus myosuroides reveals herbicide resistance pre-dated herbicides. PLoS One. 2013;8(10):e75117.CrossRefGoogle Scholar
  18. Dodsworth S, Chase MW, Kelly LJ, Leitch IJ, Macas J, Novák P, et al. Genomic repeat abundances contain phylogenetic signal. Syst Biol. 2015;64(1):112–26. Scholar
  19. Downie SR, Palmer JD. Use of chloroplast DNA rearrangements in reconstruction plant phylogeny. In: Soltis PS, et al., editors. Molecular systematics of plants. New York: Chapman and Hall; 1992. p. 1–13.Google Scholar
  20. Doyle JJ, Dickson EE. Preservation of plant species for DNA restriction endonuclease analysis. Taxon. 1987;36:715–22.CrossRefGoogle Scholar
  21. Doyle JJ, Doyle JL. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phyt Bull. 1987;19:11–5.Google Scholar
  22. Drábková L, Kirschner J, Vlcek C. Comparison of seven DNA extraction and amplification protocols in historic herbarium specimens of Juncaceae. Plant Mol Biol Rep. 2002;20:161–75.CrossRefGoogle Scholar
  23. Enan MR, Palakkott AR, Ksiksi TS. DNA barcoding of selected UAE medicinal plant species: a comparative assessment of herbarium and fresh samples. Phys Mol Biol Plants. 2017;23:221–7. Scholar
  24. Erkens RHJ, Cross H, Maas JW, Hoenselaar K, Chatrou LW. Age and greenness of herbarium specimens as predictors for successful extraction and amplification of DNA. Blumea. 2008;53:407–28.CrossRefGoogle Scholar
  25. Gansauge MT, Gerber T, Glocke I, Korlevic P, Lippik L, Nagel S, Riehl LM, Schmidt A, Meyer M. Single-stranded DNA library preparation from highly degraded DNA using T4 DNA ligase. Nucleic Acids Res. 2017;45(10):e79. Scholar
  26. Gilbert MTP, Hansen AJ, Willerslev E, Rudbeck L, Barnes I, Lynnerup N, Cooper A. Distribution patterns of postmortem damage in human mitochondrial DNA. Am J Hum Genet. 2003;72:4861. CrossRefGoogle Scholar
  27. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem. 2010;48:909–30.CrossRefGoogle Scholar
  28. Gregory TR, Nicoll JA, Tamm H, Kullman B, Kullman K, Leitch IJ, Murray BG, Kapraun DF, Greilhuber J, Bennett MD. Eukaryotic genome size databases. Nucleic Acids Res. 2007;35(Database issue):D332–D338. Scholar
  29. Gutaker RM, Reiter E, Furtwängler A, Schuenemann VJ, Burbano HA. Extraction of ultrashort DNA molecules from herbarium specimens. BioTechniques. 2017;62:76–9. Scholar
  30. Hahn C, Bachmann L, Chevreux B. Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads – a baiting and iterative mapping approach. Nucleic Acids Res. 2013;41(13):e129.CrossRefGoogle Scholar
  31. Harris SA. DNA analysis of tropical plant species: an assessment of different drying methods. Plant Syst Evol. 1993;188:57–64.Google Scholar
  32. Hart ML, Forrest LL, Nicholls JA, Kidner CA. Retrieval of hundreds of nuclear loci from herbarium specimens. Taxon. 2016;65(5):1081–92.CrossRefGoogle Scholar
  33. Heyn P, Stenzel U, Briggs AW, Kircher M, Hofreiter M, Meyer M. Road blocks on paleogenomes – polymerase extension profiling reveals the frequency of blocking lesions in ancient DNA. Nucleic Acids Res. 2010;38(16):e161. Scholar
  34. Hofreiter M, Jaenicke V, Serre D, von Haeseler A, Pääbo S. DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA. Nucleic Acids Res. 2001;29:4793–9.CrossRefGoogle Scholar
  35. Hofreiter M, Paijmans JLA, Goodchild H, Speller CF, Barlow A, Fortes GG, Thomas JA, Ludwig A, Collins MJ. The future of ancient DNA: technical advances and conceptual shifts. BioEssays. 2015;37:284–93. Scholar
  36. James SA, Soltis PS, Belbin L, Chapman AD, Nelson G, Paul DL, Collins M. Herbarium data: global biodiversity and societal botanical needs for novel research. Appl Plant Sci. 2018;6:e1024. Scholar
  37. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL. Versatile and open software for comparing large genomes. Genome Biol. 2004;5:R12. CrossRefGoogle Scholar
  38. Lindahl T. Instability and decay of the primary structure of DNA. Nature. 1993;362:709–15.CrossRefGoogle Scholar
  39. Lindahl T, Andersson A. Rate of chain breakage at apurinic sites in double-stranded deoxyribonucleic acid. Biochemistry. 1972;11:3618–23.CrossRefGoogle Scholar
  40. Litt A. Comparative evolutionary genomics of land plants. Ann Plant Rev. 2013;45:227–76. Scholar
  41. Lonardi S, Mirebrahim H, Wanamaker S, Alpert M, Ciardo G, Duma D, Close TJ. When less is more: ‘slicing’ sequencing data improves read decoding accuracy and de novo assembly quality. Bioinformatics. 2015;31:2972–80.Google Scholar
  42. Mateiu LM, Rannala BH. Bayesian inference of errors in ancient DNA caused by postmortem degradation. Mol Biol Evol. 2008;25(7):1503–11. Scholar
  43. McCabe PF, Levine A, Meijer PJ, Tapon NA, Pennell RI. A programmed cell death pathway activated in carrot cells cultured at low cell density. Plant J. 1997;12:267–80.CrossRefGoogle Scholar
  44. Mikić AM. The first attested extraction of ancient DNA in legumes (Fabaceae). Front Plant Sci. 2015;6:1006. Scholar
  45. Mohammadin S, Peterse K, van de Kerke SJ, Chatrou LW, Dönmez AA, Mummenhoff K, Pires JC, Edger PP, Al-Shehbaz IA, Schranz ME. Anatolian origins and diversification of Aethionema, the sister lineage of the core Brassicaceae. Am J Bot. 2017;104:1042–54.Google Scholar
  46. Murray BG, Leitch IJ, Bennett MD. Gymnosperm DNA C-values database. Release 4.0, Dec 2010.
  47. Olofsson JK, Bianconi M, Besnard G, Dunning LT, Lundgren MR, Holota H, Vorontsova MS, et al. Genome biogeography reveals the intraspecific spread of adaptive mutations for a complex trait. Mol Ecol. 2016;25(24):6107–123.CrossRefGoogle Scholar
  48. Osmundson TW, Robert VA, Schoch CL, Baker LJ, Smith A, Robich G, Mizzan L, Garbelotto M. Filling gaps in biodiversity knowledge for macrofungi: contributions and assessment of an herbarium collection DNA barcode sequencing project. PLoS One. 2013;8:1–8.CrossRefGoogle Scholar
  49. Pääbo S, Poinar H, Serre D, Jaenicke-Despres V, Hebler J, Rohland N, Kuch M, Krause J, Vigilant L, Hofreiter M. Genetic analyses from ancient DNA. Annu Rev Genet. 2004;38:645–79.CrossRefGoogle Scholar
  50. Pyle MM, Adams RP. In situ preservation of DNA in plant specimens. Taxon. 1989;38:576–81.CrossRefGoogle Scholar
  51. Queenborough S. Collections-based studies of plant functional traits. In: Friis I, Balslev H, editors. Tropical plant collections: legacies from the past? Essential tools for the future? Scientia Danica B (Biologica). Vol 6. 2017. p. 15–38, 223–36.Google Scholar
  52. Reape TJ, Molony EM, McCabe PF. Programmed cell death in plants: distinguishing between different modes. J Exp Bot. 2008;59:435–44.CrossRefGoogle Scholar
  53. Roldán-Arjona T, Ariza RR. Repair and tolerance of oxidative DNA damage in plants. Mutat Res. 2009;681:169–79.CrossRefGoogle Scholar
  54. Särkinen T, Staats M, Richardson JE, Cowan RS, Bakker FT. How to open the treasure chest? Optimising DNA extraction from herbarium specimens. PLoS One. 2012;7:e43808. Scholar
  55. Savolainen V, Cuénoud P, Spichiger R, Martinez MDP, Crèvecoeur M, Manen J-F. The use of hebarium specimens in DNA phylogenetics: evaluation and improvement. Plant Syst Evol. 1995;197:87–98.CrossRefGoogle Scholar
  56. Schrenk J. Schweinfurth’s method of preserving plants for herbaria. Bull Torrey Bot Club. 1888;15:292–3.CrossRefGoogle Scholar
  57. Sebastian P, Schaefer H, Telford IRH, Renner SS. Cucumber (Cucumis sativus) and melon (C. melo) have numerous wild relatives in Asia and Australia, and the sister species of melon is from Australia. PNAS. 2010;107:14269–73.CrossRefGoogle Scholar
  58. Shapiro B, Hofreiter M. A Paleogenomic perspective on evolution and gene function: new insights from ancient DNA. Science. 2014;343:1236573. Scholar
  59. Soltis PS. Digitization of herbaria enables novel research. Am J Bot. 2017;104:1–4.CrossRefGoogle Scholar
  60. Staats M, Cuence A, Richardson JE, Vrielink-van Ginkel R, Petersen G, Seberg O, Bakker FT. DNA damage in plant herbarium tissue. PLoS One. 2011;6:e28448.CrossRefGoogle Scholar
  61. Staats M, Erkens RHJ, van de Vossenberg B, Wieringa JJ, Kraaijeveld K, Stielow B, Geml J, Richardson JE, Bakker FT. Genomic treasure troves: complete genome sequencing of herbarium and insect museum specimens. PLoS One. 2013;8(7):e69189. Scholar
  62. Straub SCK, Parks M, Weitemeir K, Fishbein M, Cronn R, et al. Navigating the tip of the genomic iceberg: next-generation sequencing for plant systematics. Am J Bot. 2012;99:349–64.CrossRefGoogle Scholar
  63. Telle S, Thines M. Amplification of cox2 (~620 bp) from 2 mg of up to 129 years old herbarium specimens, comparing 19 extraction methods and 15 polymerases. PLoS One. 2008;3:e3584.CrossRefGoogle Scholar
  64. The Tomato Genome Consortium. The tomato genome sequence provides insights into fleshy fruit evolution. Nature. 2012;485:635. Scholar
  65. Turner FS. Assessment of insert sizes and adapter content in fastq data from NexteraXT libraries. Front Genet. 2014;5:1–7. Scholar
  66. Wei Z, Zhu SX, van den Berg RG, Bakker FT, Schranz ME. Phylogenetic relationships within Lactuca L. (Asteraceae), including African species, based on chloroplast DNA sequence comparisons. Genet Resour Crop Evol. 2017;64:55–71.CrossRefGoogle Scholar
  67. Weiss CL, Schuenemann VJ, Devos J, Shirsekar G, Reiter E, Gould BA, Stinchcombe JR, Krause J, Burbano HA. Temporal patterns of damage and decay kinetics of DNA retrieved from plant herbarium specimens. R Soc Open Sci. 2016;3:160239.CrossRefGoogle Scholar
  68. Welch AJ, Collins K, Ratan A, Drautz-Moses DI, Schuster SC, Lindqvist C. The quest to resolve recent radiations: plastid phylogenomics of extinct and endangered Hawaiian endemic mints (Lamiaceae). Mol Phylogenet Evol. 2016;99:16–33.CrossRefGoogle Scholar
  69. Wicke S, Schneeweiss GM. Next-generation organellar genomics: potentials and pitfalls of high-throughput technologies for molecular evolutionary studies and plant systematics. In: Hörandl E, Appelhans MS, editors. Next generation sequencing in plant systematics. Bratislava: International Association for Plant Taxonomy (IAPT); 2015. p. 9–50.Google Scholar
  70. Xu C, Dong W, Shi S, Cheng T, Li C, Liu Y, Wu P, Wu H, Gao P, Zhou S. Accelerating plant DNA barcode reference library construction using herbarium specimens: improved experimental techniques. Mol Ecol Resour. 2015;15:1366–74. Scholar
  71. Yao W, Mei C, Nan X, Hui L. Evaluation and comparison of in vitro degradation kinetics of DNA in serum, urine and saliva: a qualitative study. Gene. 2016;590(1):142–8. Epub 2016 June 16.CrossRefPubMedGoogle Scholar
  72. Yoshida K, Burbano HA, Krause J, Thines M, Weigel D, et al. Mining herbaria for plant pathogen genomes: back to the future. PLoS Pathog. 2014;10(4):e1004028. Scholar
  73. Yoshida K, Sasaki E, Kamoun S. Computational analyses of ancient pathogen DNA from herbarium samples: challenges and prospects. Front Plant Sci. 2015;6:771.CrossRefGoogle Scholar
  74. Zedane L, Hong-Wa C, Murienne J, Jeziorsky C, Baldwin BG, Besnard G. Museomics illuminate the history of an extinct, paleoendemic plant lineage (Hesperelaea, Oleaceae) known from an 1875 collection from Guadalupe Island, Mexico. Biol J Linn Soc. 2015;117:44–57.CrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Biosystematics GroupWageningen University & ResearchWageningenThe Netherlands

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