Genome evolution of ferns: Evidence for relative stasis of genome size across the fern phylogeny

New Phytologist

Volumn 210, Issue 3, 2016, Pages 1072-1082

  Clark, James ^a,b   Hidalgo, Oriane ^c   Pellicer, Jaume ^c   Liu, Hongmei ^d   Marquardt, Jeannine ^a   Robert, Yannis ^e   Christenhusz, Maarten ^c,f   Zhang, Shouzhou ^d   Gibby, Mary ^g   Leitch, Ilia J ^c   Schneider, Harald ^a,h  

^a DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c ROYAL BOTANIC GARDENS   (United Kingdom)

^d INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^e Plant Gateway ^*  (France)

^f Plant Gateway   (United Kingdom)

^g ROYAL BOTANIC GARDEN EDINBURGH   (United Kingdom)

^h SUN YAT SEN UNIVERSITY   (China)

Author keywords

Chromosome number; Chromosome structure; DNA C values; Genome size; Macroevolution; Phylogeny; Polyploidy; Pteridophytes

Indexed keywords

ANCESTRY; CHROMOSOME; CLADISTICS; DNA; FERN; GENETIC STRUCTURE; GENOME; PHYLOGENY; POLYPLOIDY; SPECIES DIVERSITY;

FILICOPHYTA; MAGNOLIOPHYTA; OSMUNDACEAE; PSILOTACEAE; PTERIDOPHYTA;

FERN; GENETICS; GENOME SIZE; MOLECULAR EVOLUTION; PHYLOGENY; PLANT CHROMOSOME; PLANT GENOME;

CHROMOSOMES, PLANT; EVOLUTION, MOLECULAR; FERNS; GENOME SIZE; GENOME, PLANT; PHYLOGENY;

EID: 84954289258     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13833     Document Type: Article

References (67)

1. Bainard J, Henry T, Bainard L, Newmaster S. 2011. DNA content variation in monilophytes and lycophytes: large genomes that are not endopolyploid. Chromosome Research 19: 763-775.
2. Barker MS. 2013. Karyotype and genome evolution in pteridophytes. In: Greilhuber J, Doležel J, Wendel JF, eds. Plant genome diversity, vol. 2. Vienna, Austria: Springer, 245-253.
3. Barker MS, Wolf PG. 2010. Unfurling fern biology in the genomics age. BioScience 60: 177-185.
4. Bellefroid E, Rambe SK, Leroux O, Viane RLL. 2010. The base number of 'loxoscaphoid' Asplenium species and its implication for cytoevolution in Aspleniaceae. Annals of Botany 106: 157-171.
5. Bennett MD, Johnston S, Hodnett GL, Price HJ. 2000. Allium cepa L. cultivars from four continents compared by flow cytometry show nuclear DNA constancy. Annals of Botany 85: 351-357.
6. Bennett MD, Leitch IJ. 2012. Pteridophyte DNA C-values database (release 5.0, Dec. 2012). [WWW document] URL http://data.kew.org/cvalues/. [accessed 1 August 2015]
7. Bomfleur B, McLoughlin S, Vajda V. 2014. Fossilized nuclei and chromosomes reveal 180 million years of genomic stasis in Royal Ferns. Science 343: 1376-1377.
8. Bou Dagher-Kharrat M, Abdel-Samad N, Douaihy B, Bourge M, Fridlender A, Siljak-Yakovlev S, Brown SC. 2013. Nuclear DNA C-values for biodiversity screening: case of the Lebanese flora. Plant Biosystems 147: 1228-1237.
9. Chang Y, Li J, Lu S, Schneider H. 2013. Species diversity and reticulate evolution in the Asplenium normale complex (Aspleniaceae) in China and adjacent areas. Taxon 62: 673-687.
10. Christenhusz MJM, Chase MW. 2014. Trends and concepts in fern classification. Annals of Botany 113: 571-594.
11. Christenhusz MJM, Zhang X-C, Schneider H. 2011. A linear sequence of extant families and genera of lycophytes and ferns. Phytotaxa 19: 7-54.
12. Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.
13. Doležel J, Binarova P, Lucretti S. 1989. Analysis of nuclear DNA content in plant cells by flow cytometry. Biologia Plantarum 31: 113-120.
14. Doležel J, Greilhuber J, Lucretti S, Meister A, Lysák MA, Nardi L, Obermayer R. 1998. Plant genome size estimation by flow cytometry: inter-laboratory comparison. Annals of Botany 82: 17-26.
15. Doležel J, Greilhuber J, Suda J. 2007. Estimation of nuclear DNA content in plants using flow cytometry. Nature Protocols 2: 2233-2244.
16. Doležel J, Sgorbati S, Lucretti S. 1992. Comparison of three DNA fluorochromes for flow cytometric estimation of nuclear DNA content in plants. Physiologia Plantarum 85: 625-631.
17. Duncan T, Smith AR. 1978. Primary basic chromosome numbers in ferns: facts or fantasies? Systematic Botany 3: 105-114.
18. Dyer R, Pellicer J, Savolainen V, Leitch I, Schneider H. 2013. Genome size expansion and the relationship between nuclear DNA content and spore size in the Asplenium monanthes fern complex (Aspleniaceae). BMC Plant Biology 13: 219.
19. Ebihara A, Ishikawa H, Matsumoto S, Lin S-J, Iwatsuki K, Takamiya M, Watano Y, Ito M. 2005. Nuclear DNA, chloroplast DNA, and ploidy analysis clarified biological complexity of the Vandenboschia radicans complex (Hymenophyllaceae) in Japan and adjacent areas. American Journal of Botany 92: 1535-1547.
20. Ekrt L, Trávníček P, Jarolímová V, Vít P, Urfus T. 2009. Genome size and morphology of the Dryopteris affinis group in Central Europe. Preslia 81: 261-280.
21. Felsenstein J. 1985. Phylogenies and the comparative method. American Naturalist 125: 1-15.
22. Garland T, Dickerman AW, Janis CM, Jones JA. 1993. Phylogenetic analysis of covariance by computer-simulation. Systematic Biology 42: 265-292.
23. Greilhuber J, Doležel J, Lysak MA, Bennett MD. 2005. The origin, evolution and proposed stabilization of the terms 'Genome size' and 'C-value' to describe nuclear DNA contents. Annals of Botany 95: 255-260.
24. Harrell FE Jr. 2014. Hmisc: Harell Miscellaneous. R package version 3.14-4. [WWW document] URL http://CRAN.R-project.org/package=Hmisc. [accessed 1 August 2015].
25. Haufler CH. 1987. Electrophoresis is modifying our concepts of evolution in homosporous pteridophytes. American Journal of Botany 74: 953-966.
26. Haufler CH. 2002. Homospory 2002: an odyssey of progress in pteridophyte genetics and evolutionary biology. BioScience 52: 1081-1093.
27. Haufler CH. 2014. Ever since Klekowski: testing a set of radical hypotheses revives the genetics of ferns and lycophytes. American Journal of Botany 101: 2036-2042.
28. Hennequin S, Ebihara A, Dubuisson J-Y, Schneider H. 2010. Chromosome number evolution in Hymenophyllum (Hymenophyllaceae), with special reference to the subgenus Hymenophyllum. Molecular Phylogenetics and Evolution 55: 47-59.
29. Henry TA, Bainard JD, Newmaster SG. 2015. Genome size evolution in Ontario ferns (Polypodiidae): evolutionary correlations with cell size, spore size, and habitat type and an absence of genome downsizing. Genome 57: 555-566.
30. Jiao YN, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang HY, Soltis PS et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-102.
31. Khandelwal S. 1990. Chromosome evolution in the genus Ophioglossum L. Botanical Journal of the Linnean Society 102: 205-217.
32. Kim HT, Chung MG, Kim K-J. 2014. Chloroplast genome evolution in early diverged leptosporangiate ferns. Molecules and Cells 37: 372-382.
33. Klekowski EJ, Baker HG. 1966. Evolutionary significance of polyploidy in the Pteridophyta. Science 153: 305-307.
34. Lehtonen S. 2011. Towards resolving the complete fern tree of life. PLoS ONE 6: e24851.
35. Leitch AR, Leitch IJ. 2012. Ecological and genetic factors linked to contrasting genome dynamics in seed plants. New Phytologist 194: 629-646.
36. Leitch IJ, Bennett MD. 2004. Genome downsizing in polyploid plants. Biological Journal of the Linnean Society 82: 651-663.
37. Leitch IJ, Leitch AR. 2013. Genome size diversity and evolution in land plants. In: Leitch IJ, Greilhuber J, Doležel J, Wendel JF, eds. Plant genome diversity, vol. 2, physical structure, behaviour and evolution of plant genomes. Wien, Austria: Springer-Verlag, 307-322.
38. Loureiro J, Rodriguez E, Doležel J, Santos C. 2007. Two new nuclear isolation buffers for plant DNA flow cytometry: a test with 37 species. Annals of Botany 100: 87-888.
39. Lovis JD. 1977. Evolutionary patterns and processes in ferns. Advances in Botanical Research 4: 229-415.
40. Maddison WP, Maddison DR. 2014. Mesquite: a modular system for evolutionary analysis. v.2.75. [WWW document] URL http://mesquiteproject.org [accessed 1 August 2015].
41. Manton I. 1950. Problems of cytology and evolution in the Pteridophyta. Cambridge, UK: Cambridge University Press.
42. Manton I, Vida G. 1968. Cytology of the fern flora of Tristan da Cunha. Proceedings of the Royal Society of London. Series B 170: 361-379.
43. Mayrose I, Barker MS, Otto SP. 2010. Probabilistic models of chromosome number evolution and the inference of polyploidy. Systematic Biology 59: 132-144.
44. Midford PE, Garland JT, Maddison WP. 2011. PDAP:PDTREE package 1.16. [WWW document] URL http://mesquiteproject.org/pdap_mesquite/index.html [accessed 1 August 2015].
45. Nakazato T, Barker MS, Rieseberg LH, Gastony GL. 2008. Evolution of the nuclear genome of ferns and lycophytes. In: Ranker TA, Haufler CH, eds. Biology and evolution of ferns and lycophytes. Cambridge, UK: Cambridge University Press, 175-198.
46. Nitta JH, Ebihara A, Ito M. 2011. Reticulate evolution in the Crepidomanes minutum species complex (Hymenophyllaceae). American Journal of Botany 98: 1782-1800.
47. Obermayer R, Leitch IJ, Hanson L, Bennett MD. 2002. Nuclear DNA C-values in 30 species double the familial representation in pteridophytes. Annals of Botany 90: 209-217.
48. Pagel M, Meade A, Barker D. 2004. Bayesian estimation of ancestral character states on phylogenies. Systematic Biology 53: 673-684.
49. Pellicer J, Leitch IJ. 2014. The application of flow cytometry for estimating genome size and ploidy level in plants. In: Besse P, ed. Molecular plant taxonomy: methods and protocols. Volume 1115. Springer Science+Business Media: New York, NY, USA, 279-307.
50. Pryer KM, Schneider H, Smith AR, Cranfill R, Wolf PG, Hunt JS, Sipes SD. 2001. Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409: 618-622.
51. Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R. 2004. Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. American Journal of Botany 91: 1582-1598.
52. Pustahija F, Brown SC, Bogunic F, Basic N, Muratovic E, Ollier S, Hidalgo O, Bourge M, Stevanovic V, Siljak-Yakovlev S. 2013. Small genomes dominate in plants growing on serpentine soils in West Balkans, an exhaustive study of 8 habitats covering 308 taxa. Plant and Soil 373: 427-453.
53. Rambaut A, Suchard MA, Xie D, Drummond AJ. 2014. Tracer v.1.6. [WWW document] URL http://beast.bio.ed.ac.uk/Tracer [accessed 1 August 2015].
54. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539-542.
55. Schneider H, Liu H, Clark J, Hidalgo O, Pellicer J, Zhang S, Kelly LJ, Fay MF, Leitch IJ. 2015. Are the genomes of royal ferns really frozen in time? Evidence for coinciding genome stability and limited evolvability in the royal ferns. New Phytologist 207: 10-13.
56. Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallon S, Lupia R. 2004. Ferns diversified in the shadow of angiosperms. Nature 428: 553-557.
57. Smith AR, Pryer KM, Schuettpelz E, Korall P, Schneider H, Wolf PG. 2006. A classification for extant ferns. Taxon 55: 705-731.
58. Soltis DE, Albert VA, Leebes-Mack J, Bell CD, Paterson AH, Zheng CF, Sankoff D, dePamphilis CW, Wall PK, Soltis PS. 2009. Polyploidiy and angiosperm diversification. American Journal of Botany 96: 336-348.
59. Soltis DE, Soltis PS. 1987. Polyploidy and breeding systems in homosporous Pteridophyta: a reevaluation. American Naturalist 130: 219-232.
60. Vanneste K, Sterck L, Myburg AA, Van de Peer Y, Mizrachi E. 2015. Horsetails are ancient polyploids: evidence from Equisetum giganteum. Plant Cell 27: 1567-1578.
61. Wagner WH, Wagner FS. 1980. Polyploidy in pteridophytes. In: Lewis WH, ed. Polyploidy: biological relevance. New York, NY, USA: Plenum Press, 199-214.
62. Wang L, X-p Qi, Xiang Q-P, Heinrichs J, Schneider H, Zhang X-C. 2010. Phylogeny of the paleotropical fern genus Lepisorus (Polypodiaceae, Polypodiopsida) inferred from four chloroplast DNA regions. Molecular Phylogenetics and Evolution 54: 211-225.
63. Webb CO, Ackerly DD, Kembel SW. 2008. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24: 2098-2100.
64. Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E, Matasci N, Ayyampalayam S, Barker MS, Burleigh JG, Gitzendanner MA et al. 2014. Phylotranscriptomic analysis of the origin and early diversification of land plants. Proceedings of the National Academy of Sciences, USA 111: E4859-E4868.
65. Williams EW, Waller DM. 2012. Phylogenetic placement of species within the genus Botrychium s.s. (Ophioglossaceae) on the basis of plastid sequences, amplified fragment length polymorphisms, and flow cytometry. International Journal of Plant Sciences 173: 516-531.
66. Wolf PG, Sessa EB, Marchant DB, Li F-W, Rothfels CJ, Sigel EM, Gitzendanner MA, Visger CJ, Banks JA, Soltis DE et al. 2015. An exploration into fern genome space. Genome Biology and Evolution 7: 2533-2544.
67. Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH. 2009. The frequency of polyploid speciation in vascular plants. Proceedings of the National Academy of Sciences, USA 106: 13875-13879.