DNA analysis of Castanea sativa (sweet chestnut) in Britain and Ireland: Elucidating European origins and genepool diversity

English version

Autoři: Rob Jarman ^aff001; Claudia Mattioni ^aff002; Karen Russell ^aff003; Frank M. Chambers ^aff001; Debbie Bartlett ^aff004; M. Angela Martin ^aff005; Marcello Cherubini ^aff002; Fiorella Villani ^aff002; Julia Webb ^aff001
Působiště autorů: Centre for Environmental Change and Quaternary Research, School of Natural & Social Sciences, University of Gloucestershire, Cheltenham, United Kingdom ^aff001; Istituto di Ricerca sugli Ecosistemi Terrestri (IRET), Consiglio Nazionale delle Ricerche, Porano, Italy ^aff002; K Russell Consulting Ltd, Leighton Bromswold, Huntingdon, United Kingdom ^aff003; Faculty of Engineering & Science, University of Greenwich, Chatham Maritime, United Kingdom ^aff004; Department of Genetics, University of Cordoba, Cordoba, Spain ^aff005
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222936

Souhrn

Castanea sativa is classified as non-indigenous in Britain and Ireland. It was long held that it was first introduced into Britain by the Romans, until a recent study found no corroborative evidence of its growing here before c. AD 650. This paper presents new data on the genetic diversity of C. sativa in Britain and Ireland and potential ancestral sources in continental Europe. Microsatellite markers and analytical methods tested in previous European studies were used to genotype over 600 C. sativa trees and coppice stools, sampled from ancient semi-natural woodlands, secondary woodlands and historic cultural sites across Britain and Ireland. A single overall genepool with a diverse admixture of genotypes was found, containing two sub groups differentiating Wales from Ireland, with discrete geographical and typological clusters. C. sativa genotypes in Britain and Ireland were found to relate predominantly to some sites in Portugal, Spain, France, Italy and Romania, but not to Greece, Turkey or eastern parts of Europe. C. sativa has come to Britain and Ireland from these western European areas, which had acted as refugia in the Last Glacial Maximum; we compare its introduction with the colonization/translocation of oak, ash, beech and hazel into Britain and Ireland. Clones of C. sativa were identified in Britain, defining for the first time the antiquity of some ancient trees and coppice stools, evincing both natural regeneration and anthropogenic propagation over many centuries and informing the chronology of the species’ arrival in Britain. This new evidence on the origins and antiquity of British and Irish C. sativa trees enhances their conservation and economic significance, important in the context of increasing threats from environmental change, pests and pathogens.

Klíčová slova:

Phylogenetic analysis – Europe – Trees – United Kingdom – Paleogenetics – Ireland – Wales – England

Zdroje

1. Jarman R, Hazell Z, Campbell G, Webb J, Chambers FM. Sweet chestnut (Castanea sativa Mill.) in Britain: re-assessment of its status as a Roman archaeophyte. Britannia. 2019;50: 1–26. doi: 10.1017/S0068113X19000011

2. Krebs P, Pezzatti GB, Beffa G, Tinner W, Conedera M. Revising the sweet chestnut (Castanea sativa Mill.) refugia history of the last glacial period with extended pollen and macrofossil evidence. Quat Sci Rev. 2019;206: 111–128. doi: 10.1016/j.quascirev.2019.01.002

3. Kremer A. Did early human populations in Europe facilitate the dispersion of oaks? Internat Oaks. 2015;26: 19–28.

4. Brown JA, Beatty GE, Montgomery WI, Provan J. Broad-scale genetic homogeneity in natural populations of common hazel (Corylus avellana) in Ireland. Tree Genet Genomes. 2016;12: 122. doi: 10.1007/s11295-016-1079-7

5. Petit R, Brewer S, Bordács S, Burg K, Cheddadi R, Coart E, et al. Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. For Ecol Manage. 2002;156: 49–74.

6. Lowe A, Unsworth C, Gerber S, Davies S, Munro R, Kelleher C, et al. Route, speed, and mode of oak postglacial colonisation across the British Isles: integrating molecular ecology, palaeoecology and modelling approaches. Bot J Scot. 2005;57(1+2): 59–81

7. Huntley B, Birks HJB. An Atlas of Past and Present Pollen Maps for Europe: 0–13,000 years ago. Cambridge: Cambridge University Press; 1983.

8. Fernandez-Cruz J, Fernandez-Lopez J. Morphological, molecular and statistical tools to identify Castanea species and their hybrids. Conserv Genet. 2012;13: 1589–1600.

9. Martin MA, Mattioni C, Cherubini M, Taurchini D, Villani F. Genetic diversity in European chestnut populations by means of genomic and genic microsatellite markers. Tree Genet Genomes. 2010;6(5): 735–744.

10. Lusini I, Velichkov I, Pollegioni P, Chiocchini F, Hinkov G, Zlatanov T, et al. Estimating the genetic diversity and spatial structure of Bulgarian Castanea sativa populations by SSRs: implication for conservation. Conserv Genet. 2014;15: 283–293.

11. Mattioni C, Martin MA, Chiocchini F, Cherubini M, Gaudet M, Pollegioni P, et al. Landscape genetics structure of European sweet chestnut (Castanea sativa Mill): indications for conservation priorities. Tree Genet Genomes. 2017;13: 1–14.

12. López-Sáez JA, Glais A, Robles-López S, Alba-Sánchez F, Pérez-Díaz S, Abel-Schaad D, et al. Unraveling the naturalness of sweet chestnut forests (Castanea sativa Mill.) in central Spain. Veg Hist Archaeobot. 2017;26: 167–182. doi: 10.1007/s00334-016-0575-x

13. Roces-Díaz JV, Jiménez-Alfaro B, Chytrý M, Díaz-Varela ER, Álvarez-Álvarez P. Glacial refugia and mid-Holocene expansion delineate the current distribution of Castanea sativa in Europe. Palaeogeogr Palaeoclimatol Palaeoecol. 2018;491: 152–160.

14. Conedera M, Krebs P, Tinner W, Pradella M, Torriani D. The cultivation of Castanea sativa (Mill.) in Europe, from its origin to its diffusion on a continental scale. Veg Hist Archaeobot. 2004;13: 161–179.

15. Pereira-Lorenzo S, Ballester A, Corredoira E, Vieitez AM, Anagnostakis S, Costa R, et al. Chestnut. In: Badenes M, Byrne D, editors. Fruit Breeding. Springer; 2012. pp. 729–769.

16. Squatriti P. Landscape and change in early medieval Italy: chestnut, economy and culture. 1st ed. Cambridge: Cambridge University Press; 2013.

17. Ledger PM, Miras Y, Poux M, Milcent PY. The palaeoenvironmental impact of prehistoric settlement and proto-historic urbanism: tracing the emergence of the oppidum of Corent, Auvergne, France. PLoS ONE 2015;10(4): e0121517. doi: 10.1371/journal.pone.0121517 25853251

18. Conedera M, Tinner W, Krebs P, de Rigo D, Caudullo G. Castanea sativa in Europe: distribution, habitat, usage and threats. In: San-Miguel-Ayanz J, de Rigo D, Caudullo G, Houston Durrant T, Mauri A, editors European Atlas of Forest Tree Species. Publ. Off. EU, Luxembourg, pp. e0125e0+; 2016.

19. Godwin H. The History of the British Flora. 2nd ed. Cambridge: Cambridge University Press; 1975.

20. Preston CD, Pearman DA, Hall AR. Archaeophytes in Britain. Bot J Linn Soc. 2004;145: 257–294. doi: 10.1111/j.1095-8339.2004.00284.x

21. Rackham O. Woodlands. London: Harper Collins, New Naturalist; 2006.

22. Stace CA, Crawley MJ. Alien plants. London: Harper Collins; 2015.

23. Rackham O. Ancient Woodland. 2nd ed. Dalbeattie: Castlepoint Press; 2003.

24. Botanical Society of Britain & Ireland. BSBI Distribution Database. Accessed 01 March 2019. Available from: https://bsbi.org/maps?taxonid=2cd4p9h.yx

25. Buckley P, Howell R. The Ecological Impact of Sweet Chestnut coppice silviculture on former ancient broadleaved woodland sites in South-east England. Research Report 627. Peterborough: English Nature; 2004.

26. NFI preliminary estimates of quantities of broadleaved species in British woodlands. National Forest Inventory Report. Edinburgh: Forestry Commission. 2013.

27. Ancient tree inventory. Grantham, UK: Woodland Trust. 2017. Available from: http://www.ancient-tree-hunt.org.uk/discoveries/TreeSearch

28. Evelyn J. Silva, or A Discourse of Forest-Trees and the Propagation of Timber in His Majesty's Dominions. 4th ed. London: Royal Society; 1706.

29. TNA: C53/76 (Ch. R. 18 Edward 1) m.10 (in an inspeximus, 1 July 1290), The National Archives, London.

30. Jarman R, Moir AK, Webb JC, Chambers FM and Russell K. Dendrochronological assessment of British veteran sweet chestnut (Castanea sativa) trees: successful cross-matching, and cross-dating with British and French oak (Quercus) chronologies. Dendrochronologia. 2018;51: 10–21. doi: 10.1016/j.dendro.2018.07.001

31. O’Sullivan Beare P. The Natural History of Ireland 1626. Translated and edited by O’Sullivan DC. Cork: Cork University Press; 2009.

32. Forbes AC. Tree Planting in Ireland during Four Centuries. Proc Roy Irish Academy. Section C: Archaeology, Celtic Studies, History, Linguistics, Literature. 1932;41: 168–199. Available from: www.jstor.org/stable/25515967.

33. Register Tree. Tree Council of Ireland. 2018. Available from: http://treecouncil.ie/treeregisterofireland/aaspecies.htm.

34. Buck EJ. Genetic variation of Castanea sativa Mill. Unpub. PhD thesis. University of Wales, Bangor. 2006.

35. Buck EJ, Hadonou M, James CJ, Blakesley D, Russell K. Isolation and characterization of polymorphic microsatellites in European chestnut (Castanea sativa Mill.). Mol Ecol Notes. 2003;3: 239–241.

36. Marinoni D, Akkak A, Bounous G, Edwards KJ, Botta R. Development and characterization of microsatellite markers in Castanea sativa (Mill.). Mol Breed. 2003;11: 127–136.

37. Barreneche T, Casasoli M, Russell K, Akkak A, Meddour H, Plomion C, et al. Comparative mapping between Quercus and Castanea using simple-sequence repeats (SSRs). Theor Appl Genet. 2004;108: 558–566. doi: 10.1007/s00122-003-1462-2 14564395

38. Mattioni C, Cherubini M, Micheli E, Villani F, Bucci G. Role of domestication in shaping Castanea sativa genetic variation in Europe. Tree Genet Genomes. 2008;4: 563–574.

39. Future Trees Trust. Available from: http://www.futuretrees.org/our-work/sweet-chestnut/current-research/.

40. Jarman R, Kofman PD. Coppice in Brief. COST Action FP1301 Reports. Freiburg: Albert Ludwig University of Freiburg. 2017. doi: 10.13140/RG.2.2.32665.42080

41. Chapuis MP, Estoup A. Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol. 2007;24: 621–631. FreeNA software. Available from: https://www1.montpellier.inra.fr/CBGP/software/FreeNA/README_FreeNA.pdf doi: 10.1093/molbev/msl191 17150975

42. Kalinowski ST. HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes. 2005;5: 187–189

43. Peakall R, Smouse PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research–an update. Bioinformatics. 2012;28: 2537–2539. doi: 10.1093/bioinformatics/bts460 22820204

44. Nei M. Analysis of gene diversity in subdivided populations. P Natl Acad Sci USA. 1973;70: 3321–3323.

45. Rousset F. Genepop on the web. Available from: https://kimura.univ-montp2.fr/~rousset/Genepop.htm.

46. Perrier X, Jacquemoud-Collet JP. DARwin software. 2006. Available from: http://darwin.cirad.fr/.

47. Queller DC, Goodnight KF. Estimating relatedness using genetic markers. Evolution. 1989;43: 258–275. doi: 10.1111/j.1558-5646.1989.tb04226.x 28568555

48. Lynch M, Ritland K. Estimation of pairwise relatedness with molecular markers. Genetics. 1999;152: 1753–1766. 10430599

49. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155: 945–959. 10835412

50. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14: 2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x 15969739

51. Earl DA, von Holdt BM. Structure Harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 2012;4: 359–361.

52. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I. CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour. 2015;15(5): 1179–1191. doi: 10.1111/1755-0998.12387 25684545

53. Sneath PHA, Sokal RR. Numerical Taxonomy. San Francisco: Freeman. 1973.

54. Takezaki N, Nei M, Tamura K. POPTREE2: software for constructing population trees from allele frequency data and computing other population statistics with windows interface. Mol Biol Evol. 2010;27: 747–752. doi: 10.1093/molbev/msp312 20022889

55. Rambaut A. FigTree, version 1.4.3. Computer program distributed by the author 04–10–2016. Available from: http://tree.bio.ed.ac.uk/software/figtree/. Cited 01 June 2018.

56. Commission Forestry. Regions of Provenance and native seed zones. Available from: https://www.forestry.gov.uk/forestry/infd-72kldl. Cited 02 May 2018.

57. Rippon S, Smart C, Pears B, Fleming F. The Fields of Britannia: continuity and discontinuity in the Pays and Regions of Roman Britain. Landscapes. 2013;14(1): 33–53.

58. Beccaro GL, Torello-Marinoni D, Binelli G, Donno D, Boccacci P, Botta R, et al. (2012). Insights in the chestnut genetic diversity in Canton Ticino (Southern Switzerland). Silvae Genetica. 2012;61(6): 292–300. doi: 10.1515/sg-2012-0037

59. Ramos-Cabrer AM, Caruncho-Picos L, Díaz-Hernández MB, Ciordia-Ara M, Rios-Mesa D, González-Díaz J, et el. Study of Spanish chestnut cultivars using SSR markers. Adv Hort Sci. 2006;20: 113–16.

60. Poljak I, Idžojtić M1, Šatović Z, Ježić M, Ćurković-Perica M, Simovski B, et al. Genetic diversity of the sweet chestnut (Castanea sativa) in Central Europe and the western part of the Balkan Peninsula and evidence of marron genotype introgression into wild populations. Tree Genet Genomes. 2017;13: 1–13.

61. Konovalov D, Heg D. A maximum-likelihood relatedness estimator allowing for negative relatedness values. Mol Ecol Resour. 2008;8(2): 256–263. doi: 10.1111/j.1471-8286.2007.01940.x 21585767

62. Miller AC, Woeste K, Anagnostakis SL, Jacobs DF. Exploration of a rare population of Chinese chestnut in North America: stand dynamics, health and genetic relationships. AoB PLANTS. 2014;6: plu065; doi: 10.1093/aobpla/plu065 25336337

63. Wang J. Estimating pairwise relatedness in a small sample of individuals. Heredity. 2017;119: 302–313. doi: 10.1038/hdy.2017.52 28853716

64. Sutherland BG, Belaj A, Nier S, Cottrell J, Vaughan SP, Hubert J, et al. Molecular biodiversity and population structure in common ash (Fraxinus excelsior L.) in Britain: implications for conservation. Mol Ecol. 2010;19: 2196–2211. doi: 10.1111/j.1365-294X.2009.04376.x 20465580

65. Harmer R. Management of coppice stools. RIN 259. Farnham: Forestry Authority. 1995.

66. Pereira-Lorenzo S, Ramos-Cabrer AM, Barreneche T, Mattioni C, Villani F, Diaz-Hernandez B, et al. Instant domestication process of European chestnut cultivars. Ann Appl Biol. 2019;174: 74–85. doi: 10.1111/aab.12474

67. Diez CM, Trujillo I, Martinez-Urdiroz N, Barranco D, Rallo L, Gaut BS. Olive domestication and diversification in the Mediterranean Basin. New Phytol. 2015;206: 436–447. doi: 10.1111/nph.13181 25420413

68. Vaughan SP, Cottrell J, Moodley DJ, Connolly T, Russell K. Clonal structure and recruitment in British wild cherry (Prunus avium). For Ecol Manage. 2007;242: 419–430.

69. Ally D, Ritland K, Otto SP. Aging in a long-lived clonal tree. PLoSBiology. 2010; 8:e1000454.

70. Pigott D. Lime-trees and basswoods. Cambridge: CUP. 2012.

71. Valbuena-Carabaña M, Gil L. Centenary coppicing maintains high levels of genetic diversity in a root resprouting oak (Quercus pyrenaica Willd.). Tree Genet Genomes. 2017;13: 28. doi: 10.1007/s11295-017-1105-4

72. Aravanopoulis FA, Drouzas AD, Paraskevi GA. Electrophoretic and quantitative variation in chestnut (Castanea sativa Mill.) in Hellenic populations in old-growth natural and coppice stands. For Snow Landsc Res. 2001;76(3): 429–434.

73. Bounous G, Marinoni D. Chestnut: botany, horticulture, and utilization. Hort Rev. 2005;31: 291–347.

74. Peeters AG, Zoller H. Long range transport of Castanea sativa pollen. Grana. 1988;27(3): 203–207. doi: 10.1080/00173138809428927

75. Cunliffe B. A race apart: insularity and connectivity. Proc Prehist Soc. 2009;75: 55–64.

76. Heuertz M, Fineschi S, Anzidei M, Pastorelli R, Salvini D, Paule L, et al. Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior L.) in Europe. Mol Ecol. 2004;13: 3437–3452. doi: 10.1111/j.1365-294X.2004.02333.x 15488002

77. Fineschi S, Salvini D, Taurchini D, Carnevale S, Vendramin GG. Chloroplast DNA variation of Tilia cordata Tiliaceae. Can J For Res. 2003;33: 2503–2508.

78. Boccacci P, Botta R. Investigating the origin of hazelnut (Corylus avellana L.) cultivars using chloroplast microsatellites. Genet Resour Crop Evol. 2009;56: 851–859. doi: 10.1007/s10722-009-9406-6

79. Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gomory D, et al. A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol. 2006;171: 199–221. doi: 10.1111/j.1469-8137.2006.01740.x 16771995

80. Sjolund MJ, Gonzalez-Diaz P, Moreno-Villena JJ, Jump AS. Understanding the legacy of widespread population translocations on the post-glacial genetic structure of the European beech, Fagus sylvatica L. J Biogeogr. 2017; 1–13. doi: 10.1111/jbi.13053

81. Packham JR, Thomas PA, Atkinson MD, Degen T. Biological Flora of the British Isles: Fagus sylvatica. J Ecol. 2012; 100: 1557–1608. doi: 10.1111/j.1365-2745.2012.02017.x

82. Benito Garzon M, Sanchez de Dios R, Sainz Ollero H. Predictive modelling of tree species distributions on the Iberian Peninsula during the Last Glacial Maximum and Mid-Holocene. Ecography. 2007;30: 120–134. doi: 10.1111/j.2006.0906–7590.04813.x

DNA analysis of Castanea sativa (sweet chestnut) in Britain and Ireland: Elucidating European origins and genepool diversity

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz