Global DNA cytosine methylation as an evolving trait: Phylogenetic signal and correlated evolution with genome size in angiosperms

Frontiers in Genetics

Volumn 5, Issue JAN, 2015, Pages

  Alonso, Conchita ^a   Pérez, Ricardo ^b   Bazaga, Pilar ^a   Herrera, Carlos M ^a  

^a DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^b CSIC JA USE Centro de Investigaciones Cientificas Isla de la Cartuja CICIC   (Spain)

Author keywords

Angiosperms; C value; Correlated evolution; DNA cytosine methylation; Epigenetics; Genome size; HPLC; Phylogenetic signal

Indexed keywords

CYTOSINE;

ANALYTIC METHOD; ANGIOSPERM; ARABIDOPSIS THALIANA; ARTICLE; CELL LINEAGE; DNA CYTOSINE METHYLATION; DNA EXTRACTION; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; GENE MUTATION; GENETIC DATABASE; GENETIC HETEROGENEITY; GENETIC VARIABILITY; GENOME SIZE; GENOMIC INSTABILITY; GENOTYPE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MAIZE; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NARCISSUS; NONHUMAN; PHYLOGENETIC TREE; QUANTITATIVE TRAIT; RANDOMIZATION; RICE; SIGNAL TRANSDUCTION;

ARABIDOPSIS; EUKARYOTA; MAGNOLIOPHYTA; NARCISSUS;

EID: 84923169323     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2015.00004     Document Type: Article

References (74)

1. Banks, J., and Federoff, N. (1989). Patterns of developmental and heritable change in methylation of the suppressor-mutator transposable element. Dev. Genet. 10, 425-437. doi: 10.1002/dvg.1020100604
2. Bender, J. (2004). DNA methylation and epigenetics. Ann. Rev. Plant Biol. 55, 41-68. doi: 10.1146/annurev.arplant.55.031903.141641
3. Bennett, M., and Leitch, I. (2005). "Genome size evolution in plants," in The Evolution of the Genome, ed T. R. Gregory (Amsterdam: Elsevier), 89-162.
4. Bennett, M., and Leitch, I. (2012). Angiosperm DNA C-values Database (Release 8.0, December 2012). Available online at: http://www.kew.org/cvalues/
5. Bennetzen, J., Sanmiguel, P., Chen, M., Tikhonov, A., Francki, M., and Avramova, Z. (1998). Grass genomes. Proc. Natl. Acad. Sci. U.S.A. 95, 1975-1978. doi: 10.1073/pnas.95.5.1975
6. Bird, A. (1995). Gene number, noise reduction and biological complexity. Trends Genet. 11, 94-100. doi: 10.1016/S0168-9525(00)89009-5
7. Blomberg, S., and Garland, T. (2002). Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. J. Evol. Biol. 15, 899-910. doi: 10.1046/j.1420-9101.2002.00472.x
8. Blomberg, S., Garland, T., and Ives, A. (2003). Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717-745. doi: 10.1554/0014-3820(2003)057[0717:TFPSIC]2.0.CO;2
9. Bonchev, G., and Parisod, C. (2013). Transposable elements and microevolutionary changes in natural populations. Mol. Ecol. Res. 13, 765-775. doi: 10.1111/1755-0998.12133
10. Choi, C., and Sano, H. (2007). Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Mol. Genet. Genomics 277, 589-600. doi: 10.1007/s00438-007-0209-1
11. Cokus, S., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C., et al. (2008). Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215-219. doi: 10.1038/nature06745
12. Colot, V., and Rossignol, J. (1999). Eukaryotic DNA methylation as an evolutionary device. Bioessays 21, 402-411. doi: 10.1002/(SICI)1521-1878(199905)21:5%3C402::AID-BIES7%3E3.3.CO;2-2
13. Díaz-Uriarte, R., and Garland, T. (1996). Testing hypotheses of correlated evolution using phylogenetically independent contrasts: sensitivity to deviations from Brownian motion. Syst. Biol. 45, 27-47. doi: 10.1093/sysbio/45.1.27
14. Federoff, N. (2000). Transposons and genome evolution in plants. Proc. Natl. Acad. Sci. U.S.A. 97, 7002-7007. doi: 10.1073/pnas.97.13.7002
15. Federoff, N. (2012). Transposable elements, epigenetics, and genome evolution. Science 338, 758-767. doi: 10.1126/science.338.6108.758
16. Felsenstein, J. (1985). Phylogenies and the comparative method. Am. Nat. 125, 1-15. doi: 10.1086/284325
17. Feschotte, C., and Pritham, E. (2007). DNA transposons and the evolution of eukaryotic genomes. Annu. Rev. Genet. 41, 331-368. doi: 10.1146/annurev.genet.40.110405.090448
18. Finnegan, E., Genger, R., Kovac, K., Peacock, W., and Dennis, E. (1998a). DNA methylation and the promotion of flowering by vernalization. Proc. Natl. Acad. Sci. U.S.A. 95, 5824-5829. doi: 10.1073/pnas.95.10.5824
19. Finnegan, E., Genger, R., Peacock, W., and Dennis, E. (1998b). DNA methylation in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 49, 223-247. doi: 10.1146/annurev.arplant.49.1.223
20. Finnegan, E., Peacock, W., and Dennis, E. (2000). DNA methylation, a key regulator of plant development and other processes. Curr. Opin. Genet. Dev. 10, 217-223. doi: 10.1016/S0959-437X(00)00061-7
21. Fraga, M., and Esteller, M. (2002). DNA methylation: a profile of methods and applications. Biotechniques 33, 632-649.
22. Freckleton, R. (2009). The seven deadly sins of comparative analysis. J. Evol. Biol. 22, 1367-1375. doi: 10.1111/j.1420-9101.2009.01757.x
23. Gorelick, R. (2003). Evolution of dioecy and sex chromosomes via methylation driving Muller's ratchet. Biol. J. Linn. Soc. 80, 353-368. doi: 10.1046/j.1095-8312.2003.00244.x
24. Grant-Downton, R., and Dickinson, H. (2005). Epigenetics and its implications for plant biology. 1. The epigenetic network in plants. Ann. Bot. 96, 1143-1164. doi: 10.1093/aob/mci273
25. Gregory, T. (2005). The C-value enigma in plants and animals: a review of parallels and an appeal for partnership. Ann. Bot. 95, 133-146. doi: 10.1093/aob/mci009
26. Grover, C., and Wendel, J. (2010). Recent insights into mechanisms of genome size change in plants. J. Bot. 2010:382732. doi: 10.1155/2010/382732
27. Haberer, G., Young, S., Bharti, A., Gundlach, H., Raymond, C., Fuks, G., et al. (2005). Structure and architecture of the maize genome. Plant Physiol 139, 1612-1624. doi: 10.1104/pp.105.068718
28. Harvey, P., and Pagel, M. (1991). The Comparative Method in Evolutionary Biology. Oxford: Oxford Univ. Press.
29. Herrera, C. M., and Bazaga, P. (2011). Untangling individual variation in natural populations: ecological, genetic and epigenetic correlates of long-term inequality in herbivory. Mol. Ecol. 20, 1675-1688. doi: 10.1111/j.1365-294X.2011.05026.x
30. Herrera, C. M., Medrano, M., and Bazaga, P. (2013). Epigenetic differentiation persists after male gametogenesis in natural populations of the perennial herb Helleborus foetidus (Ranunculaceae). PLoS ONE 8:e70730. doi: 10.1371/journal.pone.0070730
31. Herrera, C. M., Medrano, M., and Bazaga, P. (2014). Variation in DNA methylation transmissibility, genetic heterogeneity and fecundity-related traits in natural populations of the perennial herb Helleborus foetidus. Mol. Ecol. 23, 1085-1095. doi: 10.1111/mec.12679
32. Jablonka, E. (2013). Epigenetic inheritance and plasticity: the responsive germline. Prog. Biophys. Mol. Biol. 111, 99-107. doi: 10.1016/j.pbiomolbio.2012.08.014
33. Jablonka, E., and Raz, G. (2009). Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 84, 131-176. doi: 10.1086/598822
34. Johannes, F., Porcher, E., Teixeira, F., Saliba-Colombani, V., Simon, M., Agier, N., et al. (2009). Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genetics 5:e1000530. doi: 10.1371/journal.pgen.1000530
35. Jombart, T., Balloux, F., and Dray, S. (2010). adephylo: new tools for investigating the phylogenetic signal in biological traits. Bioinformatics 26, 1907-1909. doi: 10.1093/bioinformatics/btq292
36. Jones, P., Rideout, W., Shen, J., Spruck, C., and Tsai, Y. (1992). Methylation, mutation and cancer. Bioessays 14, 33-36. doi: 10.1002/bies.950140107
37. Kang, M., Tao, J., Wang, J., Ren, C., Qi, Q., Xiang, Q.-Y., et al. (2014). Adaptive and nonadaptive genome size evolution in Karst endemic flora of China. New Phytol. 202, 1371-1381. doi: 10.1111/nph.12726
38. Le, Q., Wright, S., Yu, Z., and Bureau, T. (2000). Transposon diversity in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 97, 7376-7381. doi: 10.1073/pnas.97.13.7376
39. Leitch, I., and Leitch, A. (2013). "Genome size diversity and evolution in land plants" in Plant Genome Diversity, Vol. 2. Physical Structure, Behaviour and Evolution of Plant Genomes, eds J. Greilhuber, J. Dolezel and J. F. Wendel. (New York, NY: Springer), 307-322.
40. Lisanti, S., Omar, W., Tomaszewski, B., De Prins, S., Jacobs, G., Koppen, G., et al. (2013). Comparison of methods for quantification of global DNA methylation in human cells and tissues. PLoS ONE 8:e79044. doi: 10.1371/journal.pone.0079044
41. Lister, R., O'malley, R., Tonti-Filippini, J., Gregory, B., Berry, C., Millar, A., et al. (2008). Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133, 523-536. doi: 10.1016/j.cell.2008.03.029
42. Lopez Torres, A., Yanez Barrientos, E., Wrobel, K., and Wrobel, K. (2011). Selective derivatization of cytosine and methylcytosine moieties with 2-bromoacetophenone for submicrogram DNA methylation analysis by reversed phase HPLC with spectrofluorimetric detection. Anal. Chem. 83, 7999-8005. doi: 10.1021/ac2020799
43. Martin, A., Troadec, C., Boualem, A., Rajab, M., Fernandez, R., Morin, H., et al. (2009). A transposon-induced epigenetic change leads to sex determination in melon. Nature 461, 1135-1138. doi: 10.1038/nature08498
44. McClintock, B. (1984). The significance of responses of the genome to challenge. Science 226, 792-801. doi: 10.1126/science.15739260
45. Messeguer, R., Ganal, M., Steffens, J., and Tanksley, S. (1991). Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA. Plant Mol. Biol. 16, 753-770. doi: 10.1007/BF00015069
46. Münkemüller, T., Lavergne, S., Bzeznik, B., Dray, S., Jombart, T., Schiffers, K., et al. (2012). How to measure and test phylogenetic signal. Methods Ecol. Evol. 3, 743-756. doi: 10.1111/j.2041-210X.2012.00196.x
47. Nachman, M., and Crowell, S. (2000). Estimate of the mutation rate per nucleotide in humans. Genetics 156, 297-304.
48. Nei, M. (2013). Mutation-Driven Evolution. Oxford: Oxford University Press.
49. Ossowski, S., Schneeberger, K., Lucas-Lledo, J., Warthmann, N., Clark, R., Shaw, R., et al. (2010). The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327, 92-94. doi: 10.1126/science.1180677
50. Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature 401, 877-884. doi: 10.1038/44766
51. Paradis, E. (2012). Analysis of Phylogenetics and Evolution with R, 2nd Edn. New York, NY: Springer.
52. Paun, O., Bateman, R., Fay, M., Hedren, M., Civeyrel, L., and Chase, M. (2010). Stable epigenetic effects impact adaptation in allopolyploid orchids (Dactylorhiza: Orchidaceae). Mol. Biol. Evol. 27, 2465-2473. doi: 10.1093/molbev/msq150
53. Popescu, A., Huber, K., and Paradis, E. (2012). ape 3.0: new tools for distance-based phylogenetics and evolutionary analysis in R. Bioinformatics 28, 1536-1537. doi: 10.1093/bioinformatics/bts,184
54. Rabinowicz, P., Citek, R., Budiman, M., Nunberg, A., Bedell, J., Lakey, N., et al. (2005). Differential methylation of genes and repeats in land plants. Genome Res. 15, 1431-1440. doi: 10.1101/gr.4100405
55. Rabinowicz, P., Palmer, L., May, B., Hemann, M., Lowe, S., Mccombie, R., et al. (2003). Genes and transposons are differentially methylated in plants, but not in mammals. Genome Res. 13, 2658-2664. doi: 10.1101/gr.1784803
56. R Core Team (2013). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
57. Revell, L. (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217-223. doi: 10.1111/j.2041-210X.2011.00169.x
58. Revell, L., Harmon, L., and Collar, D. (2008). Phylogenetic signal, evolutionary process, and rate. Syst. Biol. 57, 591-601. doi: 10.1080/10635150802302427
59. Rozhon, W., Baubec, T., Mayerhofer, J., Scheid, O., and Jonak, C. (2008). Rapid quantification of global DNA methylation by isocratic cation exchange high-performance liquid chromatography. Anal. Biochem. 375, 354-360. doi: 10.1016/j.ab.2008.01.001
60. SanMiguel, P., Gaut, B., Tikhonov, A., Nakajima, Y., and Bennetzen, J. (1998). The paleontology of intergene retrotransposons of maize. Nat. Genet. 20, 43-45. doi: 10.1038/1695
61. Sano, H., Kamada, I., Youssefian, S., Katsumi, M., and Wabiko, H. (1990). A single treatment of rice seedlings with 5-azacytidine induces heritable dwarfism and undermethylation of genomic DNA. Mol. Gen. Genet. 220, 441-447. doi: 10.1007/BF00391751
62. Schmitz, R., and Ecker, J. (2012). Epigenetic and epigenomic variation in Arabidopsis thaliana. Trends Plant Sci. 17, 149-154. doi: 10.1016/j.tplants.2012.01.001
63. Steward, N., Ito, M., Yamaguchi, Y., Koizumi, N., and Sano, H. (2002). Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress. J. Biol. Chem. 277, 37741-37746. doi: 10.1074/jbc.M204050200
64. Takuno, S., and Gaut, B. (2013). Gene body methylation is conserved between plant orthologs and is of evolutionary consequence. Proc. Natl. Acad. Sci. U.S.A. 110, 1797-1802. doi: 10.1073/pnas.1215380110
65. Vaughn, M., Tanurdzic, M., Lippman, Z., Jiang, H., Carrasquillo, R., Rabinowicz, P., et al. (2007). Epigenetic natural variation in Arabidopsis thaliana. PLoS Biol. 5:e174. doi: 10.1371/journal.pbio.0050174
66. Vergeer, P., Wagemaker, N., and Ouborg, N. (2012). Evidence for an epigenetic role in inbreeding depression. Biol. Lett. 8, 798-801. doi: 10.1098/rsbl.2012.0494
67. Verhoeven, K., Jansen, J., Van Dijk, P., and Biere, A. (2010). Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol. 185, 1108-1118. doi: 10.1111/j.1469-8137.2009.03121.x
68. Vesely, P., Bures, P., and Smarda, P. (2013). Nutrient reserves may allow for genome size increase: evidence from comparison of geophytes and their sister non-geophytic relatives. Ann. Bot. 112, 1193-1200. doi: 10.1093/aob/mct185
69. Wagner, I., and Capesius, I. (1981). Determination of 5-methylcytosine from plant DNA by high-performance liquid chromatography. Biochim. Biophys. Acta 654, 52-56. doi: 10.1016/0005-2787(81)90135-0
70. Webb, C., Ackerly, D., and Kembel, S. (2008). Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24, 2098-2100. doi: 10.1093/bioinformatics/btn358
71. Webb, C., and Donoghue, M. (2005). Phylomatic: tree assembly for applied phylogenetics. Mol. Ecol. Notes 5, 181-183. doi: 10.1111/j.1471-8286.2004.00829.x
72. Zemach, A., Mcdaniel, I., Silva, P., and Zilberman, D. (2010). Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328, 916-919. doi: 10.1126/science.1186366
73. Zhong, S., Fei, Z., Chen, Y.-R., Zheng, Y., Huang, M., Vrebalov, J., et al. (2013). Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat. Biotechnol. 31, 154-159. doi: 10.1038/nbt.2462
74. Zonneveld, B. J. M. (2008). The systematic value of nuclear DNA content for all species of Narcissus L. (Amaryllidaceae). Plant Syst. Evol. 275, 109-132. doi: 10.1007/s00606-008-0015-1