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Tree Genetics & Genomes

, 15:15 | Cite as

Linking DNA methylation with performance in a woody plant species

  • Rafael G. AlbaladejoEmail author
  • Clara Parejo-Farnés
  • Encarnación Rubio-Pérez
  • Sofia Nora
  • Abelardo Aparicio
Original Article
  • 30 Downloads
Part of the following topical collections:
  1. Genome Biology

Abstract

Epigenetic factors are increasingly being viewed as important mechanisms in organism performance. However, advances in plant epigenetics rely mostly on studies of short-lived model or cultivated species and there is a current gap in knowledge on wild plants, especially on woody plant species, that still needs to be addressed via empirical studies. Through a greenhouse experiment we compared the genetic (microsatellites) and epigenetic (methylation-sensitive amplified polymorphisms) variation in mother plants and their open-pollinated offspring of the Mediterranean woody plant Pistacia lentiscus. We also assessed whether the inherited DNA methylation patterns were related to the early offspring performance. Our results revealed (i) higher levels of relative DNA methylation in mother plants than in their offspring, although the amount of methylation in the offspring was remarkable; (ii) a significant relationship between relative methylation levels between the two life stages; (iii) a high epigenetic structure among families that was decoupled to the genetic structure; and (iv) a significant relationship between the relative DNA methylation levels and seedling phenotypic trait variation with higher levels of methylation in the genome being associated to a poorer performance. Our results stress the impact that epigenetic inheritance might have in evolution through its influence in seedling development, and that epigenetic effects can be detected even at early stages of the life cycle of woody long-lived species.

Keywords

DNA methylation Ecological epigenetics Epigenetic structure Methylation-sensitive amplified polymorphism (MSAP) Offspring performance Transgenerational epigenetic inheritance 

Notes

Acknowledgements

The authors thank Clara de Vega, Carlos M. Herrera, and two anonymous reviewers for their useful comments on earlier versions of this manuscript; Jose María Higuera and Jesus García from “Servicio General de Invernadero” at the Universidad de Sevilla for the greenhouse assistance; and Michael Lockwood for reviewing the English style.

Data archiving statement

Genetic and epigenetic molecular datasets as well as seedling performance measurements. Datasets have been placed in the Dryad Digital Repository with number:  https://doi.org/10.5061/dryad.gg3g3s5

Funding information

This study was funded by a project of the Spanish “Ministerio de Ciencia e Innovación” (CGL2011-23721) to AAM.

Supplementary material

11295_2019_1325_MOESM1_ESM.pdf (221 kb)
ESM 1 (PDF 221 kb)

References

  1. Albaladejo RG, Sebastiani F, Aparicio A, Buonamici A, González-Martínez SC, Vendramin GG (2008) Development and characterization of eight polymorphic microsatellite loci from Pistacia lentiscus L. (Anacardiaceae). Mol Ecol Resour 8:904–906CrossRefGoogle Scholar
  2. Albaladejo RG, Guzmán B, González-Martínez SC, Aparicio A (2012) Extensive pollen flow but few pollen donors and high reproductive variance in an extremely fragmented landscape. PLoS One 7:e49012CrossRefGoogle Scholar
  3. Alonso C, Pérez R, Bazaga P, Medrano M, Herrera CM (2016) MSAP markers and global cytosine methylation in plants: a literature survey and comparative analysis for a wild-growing species. Mol Ecol Resour 16:80–90CrossRefGoogle Scholar
  4. Angers B, Castonguay E, Massicotte R (2010) Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after. Mol Ecol 19:1283–1295CrossRefGoogle Scholar
  5. Avramidou EV, Ganopoulos IV, Doulis AG, Tsaftaris AS, Aravanopoulos FA (2015a) Beyond population genetics: natural epigenetic variation in wild cherry (Prunus avium). Tree Genet Genomes 11:95CrossRefGoogle Scholar
  6. Avramidou EV, Doulis AG, Aravanopoulos FA (2015b) Determination of epigenetic inheritance, genetic inheritance, and estimation of genome DNA methylation in a full-sib family of Cupressus sempervirens L. Gene 562:180–187CrossRefGoogle Scholar
  7. Balao F, Paun O, Alonso C (2018) Uncovering the contribution of epigenetics to plant phenotypic variation in Mediterranean ecosystems. Pl Biol 20:38–49CrossRefGoogle Scholar
  8. Bartels A, Han Q, Nair P, Stacey L, Gaynier H, Mosley M, Huang Q, Pearson J, Hsieh TF, An YQ, Xiao W (2018) Dynamic DNA methylation in plant growth and development. Int J Mol Sci 19:2144CrossRefGoogle Scholar
  9. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67:1–48CrossRefGoogle Scholar
  10. de Bello F, Lavorel S, Díaz S, Harrington R, Cornelissen JHC, Bardgett RD, Berg MP, Cipriotti P, Feld CK, Hering D, Martins da Silva P, Potts SG, Sandin L, Sousa JP, Storkey J, Wardle DA, Harrison PA (2010) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers Conserv 19:2873–2893CrossRefGoogle Scholar
  11. Bonduriansky R, Day T (2009) Nongenetic inheritance and its evolutionary implications. Annu Rev Ecol Evol S 40:103–125CrossRefGoogle Scholar
  12. Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115PubMedGoogle Scholar
  13. Bräutigam K, Vining KJ, Lafon-Placette C, Fossdal CG, Mirouze M, Marcos JG, Fluch S, Fraga MF, Guevara MÁ, Abarca D, Johnsen Ø, Maury S, Strauss SH, Campbell MM, Rohde A, Díaz-Sala C, Cervera MT (2013) Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecol Evol 3:399–415CrossRefGoogle Scholar
  14. Canadell J, Zedler PH (1995) Underground structures of woody plants in Mediterranean ecosystems of Australia, California and Chile. In: Arroyo MTK, Zedler PH, Fox MD (eds) Ecology and biogeography of Mediterranean ecosystems in Chile. California and Australia. Springer-Verlag, New York, pp 177–210Google Scholar
  15. Cendán C, Sampedro L, Zas R (2013) The maternal environment determines the timing of germination in Pinus pinaster. Environ Exp Bot 94:66–72CrossRefGoogle Scholar
  16. Cervera M, Ruiz-García L, Martínez-Zapater J (2002) Analysis of DNA methylation in Arabidopsis thaliana based on methylation-sensitive AFLP markers. Mol Gen Genomics 268:543–552CrossRefGoogle Scholar
  17. Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–161CrossRefGoogle Scholar
  18. Donohue K (2009) Completing the cycle: maternal effects as the missing link in plant life histories. Philos Trans Royal Soc B 364:1059–1074CrossRefGoogle Scholar
  19. Finnegan EJ, Peacock WJ, Dennis ES (1996) Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. P Natl Acad Sci USA 93:8449–8454CrossRefGoogle Scholar
  20. Finnegan EJ, Genger RK, Kovac K, Peacock WJ, Dennis ES (1998) DNA methylation and the promotion of flowering by vernalization. P Natl Acad Sci USA 95:5824–5829CrossRefGoogle Scholar
  21. Foust CM, Preite V, Schrey AW, Alvarez M, Robertson MH, Verhoeven KJF, Richards CL (2016) Genetic and epigenetic differences associated with environmental gradients in replicate populations of two salt marsh perennials. Mol Ecol 25:1639–1652CrossRefGoogle Scholar
  22. Fulneček J, Kovařík A (2014) How to interpret methylation sensitive amplified polymorphism (MSAP) profiles? BMC Genet 15:2CrossRefGoogle Scholar
  23. Grant-Downton RT, Dickinson HG (2006) Epigenetics and its implications for plant biology 2. The “epigenetic epiphany”: epigenetics, evolution and beyond. Ann Bot 97:11–27CrossRefGoogle Scholar
  24. Groot MP, Wagemaker N, Ouborg NJ, Verhoeven KJF, Vergeer P (2018) Epigenetic population differentiation in field- and common garden-grown Scabiosa columbaria plants. Ecol Evol 8:3505–3517CrossRefGoogle Scholar
  25. Herrera CM, Bazaga P (2010) Epigenetic differentiation and relationship to adaptive genetic divergence in discrete populations of the violet Viola cazorlensis. New Phytol 187:867–876CrossRefGoogle Scholar
  26. Herrera CM, Bazaga P (2011) Untangling individual variation in natural populations: ecological, genetic and epigenetic correlates of long-term inequality in herbivory. Mol Ecol 20:1675–1688CrossRefGoogle Scholar
  27. Herrera CM, Bazaga P (2013) Epigenetic correlates of plant phenotypic plasticity: DNA methylation differs between prickly and nonprickly leaves in heterophyllous Ilex aquifolium (Aquifoliaceae) trees. Bot J Linn Soc 171:441–452CrossRefGoogle Scholar
  28. Herrera CM, Bazaga P (2016) Genetic and epigenetic divergence between disturbed and undisturbed subpopulations of a Mediterranean shrub: a 20-year field experiment. Ecol Evol 6:3832–3847CrossRefGoogle Scholar
  29. Herrera CM, Medrano M, Bazaga P (2013) Epigenetic differentiation persists after male gametogenesis in natural populations of the perennial herb Helleborus foetidus (Ranunculaceae). PLoS One 8:e70730CrossRefGoogle Scholar
  30. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  31. Hilbert DW, Canadell J (1995) Biomass partioning and resource allocation of plants from Mediterranean-type ecosystems: possible responses to elevated atmospheric CO2. In: Moreno JM, Oechel WC (eds) Global change and Mediterranean-type ecosystems. Springer-Verlag, New York, pp 76–101CrossRefGoogle Scholar
  32. Jablonka E, Lamb MJ (2005) Evolution in four dimensions. MIT Press, CambridgeGoogle Scholar
  33. Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84:131–176CrossRefGoogle Scholar
  34. Johnsen Ø, Fossdal CG, Nagy N, Mølmann J, Dæhlen OG, Skrøppa T (2005) Climatic adaptation in Picea abies progenies is affected by the temperature during zygotic embryogenesis and seed maturation. Plant Cell Environ 28:1090–1102CrossRefGoogle Scholar
  35. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405CrossRefGoogle Scholar
  36. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94CrossRefGoogle Scholar
  37. Kakutani T (2002) Epi-alleles in plants: inheritance of epigenetic information over generations. Plant Cell Physiol 43:1106–1111CrossRefGoogle Scholar
  38. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Soft 82:1–26CrossRefGoogle Scholar
  39. Li A, Song W-Q, Chen C-B, Zhou Y-N, Qi L-W, Wang C-G (2013) DNA methylation status is associated with the formation of heterosis in Larix kaempferi intraspecific hybrids. Mol Breeding 31:463–475CrossRefGoogle Scholar
  40. Lira-Medeiros CF, Parisod C, Fernandes RA, Mata CS, Cardoso MA, Gomes-Ferreira PC (2010) Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS One 5:e10326CrossRefGoogle Scholar
  41. Lloret F, Casanovas C, Peñuelas J (1999) Seedling survival of Mediterranean shrubland species in relation to root:shoot ratio, seed size and water and nitrogen use. Funct Ecol 13:210–216CrossRefGoogle Scholar
  42. Ma K, Song Y, Jiang X, Zhang Z, Li B, Zhang D (2012) Photosynthetic response to genome methylation affects the growth of Chinese white poplar. Tree Genet Genomes 8:1407–1421CrossRefGoogle Scholar
  43. Nora S, Albaladejo RG, Aparicio A (2015) Genetic variation and structure in the Mediterranean shrubs Myrtus communis and Pistacia lentiscus in different landscape contexts. Pl Biol 17:311–319CrossRefGoogle Scholar
  44. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, et al. (2013) vegan: community ecology package. R package version 2.0–10Google Scholar
  45. Oosterhout CV, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  46. Pan D, Bouchard A, Legendre P, Domon G (1998) Influence of edaphic factors on the spatial structure of inland halophytic communities: a case study in China. J Veg Sci 9:797–804CrossRefGoogle Scholar
  47. Parejo-Farnés C, Robledo-Arnuncio JJ, Albaladejo RG, Rubio-Pérez E, Aparicio A (2017) Effects of habitat fragmentation on parental correlations in the seed rain of a bird-dispersed species. Tree Genet Genomes 13:17CrossRefGoogle Scholar
  48. Parejo-Farnés C, Albaladejo RG, Camacho C, Aparicio A (2018) From species to individuals: combining barcoding and microsatellite analyses from non-invasive samples in plant ecology studies. Pl Ecol 219:1151–1158CrossRefGoogle Scholar
  49. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539CrossRefGoogle Scholar
  50. Pérez-Figueroa A (2013) msap: a tool for the statistical analysis of methylation-sensitive amplified polymorphism data. Mol Ecol Resour 13:522–527CrossRefGoogle Scholar
  51. Platt A, Gugger P, Sork V (2015) Genome-wide signature of local adaptation linked to variable CpG methylation in oak populations. Mol Ecol 24:3823–3830CrossRefGoogle Scholar
  52. Preite V, Snoek LB, Oplaat C, Biere A, van der Putten WH, Verhoeven KJF (2015) The epigenetic footprint of poleward range-expanding plants in apomictic dandelions. Mol Ecol 24:4406–4418CrossRefGoogle Scholar
  53. Raj S, Brautigam K, Hamanishi ET, Wilkins O, Thomas BR, Schroeder W, Mansfield SD, Plant AL, Campbell MM (2011) Clone history shapes Populus drought responses. Proc Natl Acad Sci U S A 108:12521–12526CrossRefGoogle Scholar
  54. Reyna-López GE, Simpson J, Ruiz-Herrera J (1997) Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Mol Gen Genet 253:703–710CrossRefGoogle Scholar
  55. Richards EJ (2006) Inherited epigenetic variation – revisiting soft inheritance. Nat Rev Genet 7:395–401CrossRefGoogle Scholar
  56. Richards EJ (2008) Population epigenetics. Curr Opin Genet Dev 18:221–226CrossRefGoogle Scholar
  57. Richards CL, Schrey AW, Pigliucci M (2012) Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation. Ecol Lett 15:1016–1025CrossRefGoogle Scholar
  58. Rico L, Ogaya R, Barbeta A, Peñuelas J (2014) Changes in DNA methylation fingerprint of Quercus ilex trees in response to experimental field drought simulating projected climate change. Pl Biol 16:419–427CrossRefGoogle Scholar
  59. Roach DA, Wulff RD (1987) Maternal effects in plants. Annu Rev Ecol Syst 18:209–235CrossRefGoogle Scholar
  60. Rousset F (2008) Genepop’ 007: a complete re-implementation of the genepop software for windows and Linux. Mol Ecol Notes 8:103–106CrossRefGoogle Scholar
  61. Sáez-Laguna E, Guevara MA, Diáz LM, Sánchez-Gómez D, Collada C, Aranda I, Cervera MT (2014) Epigenetic variability in the genetically uniform forest tree species Pinus pinea L. PLoS One 9:e103145CrossRefGoogle Scholar
  62. Salmon A, Clotault J, Jenczewski E, Chable V, Manzanares-Dauleux MJ (2008) Brassica oleracea displays a high level of DNA methylation polymorphism. Plant Sci 174:61–70CrossRefGoogle Scholar
  63. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234CrossRefGoogle Scholar
  64. Schulz B, Eckstein RL, Durka W (2013) Scoring and analysis of methylation-sensitive amplification polymorphisms for epigenetic population studies. Mol Ecol Resour 13:642–653CrossRefGoogle Scholar
  65. Schulz B, Eckstein RL, Durka W (2014) Epigenetic variation reflects dynamic habitat conditions in a rare floodplain herb. Mol Ecol 23:3523–3537CrossRefGoogle Scholar
  66. Trucchi E, Mazzarella AB, Gilfillan GD, Lorenzo MT, Schönswetter P, Paun O (2016) BsRADseq: screening DNA methylation in natural populations of non-model species. Mol Ecol 25:1697–1713CrossRefGoogle Scholar
  67. Vekemans X, Beauwens T, Lemaire M, Roldán-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151CrossRefGoogle Scholar
  68. Vergeer P, Wagemaker N, Ouborg NJ (2012) Evidence for an epigenetic role in inbreeding depression. Biol Lett 8:798–801CrossRefGoogle Scholar
  69. Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol 185:1108–1118CrossRefGoogle Scholar
  70. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M et al (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414CrossRefGoogle Scholar
  71. Yakovlev I, Fossdal CG, Skrøppa T, Olsen JE, Jahren AH, Johnsen Ø (2012) An adaptive epigenetic memory in conifers with important implications for seed production. Seed Sci Res 22:63–76CrossRefGoogle Scholar
  72. Zhang MS, Yan HY, Zhao N, Lin XY, Pang JS, Xu KZ, Liu LX, Liu B (2007) Endosperm-specific hypomethylation, and meiotic inheritance and variation of DNA methylation level and pattern in sorghum (Sorghum bicolor L.) inter-strain hybrids. Theor Appl Genet 115:195–207CrossRefGoogle Scholar
  73. Zhang YY, Fischer M, Colot V, Bossdorf O (2013) Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol 197:314–322CrossRefGoogle Scholar
  74. Zhu J, Kapoor A, Sridhar VV, Agius F, Zhu JK (2007) The DNA glycosylase/lyase ROS1 functions in pruning DNA methylation patterns in Arabidopsis. Curr Biol 17:54–59CrossRefGoogle Scholar
  75. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, LondonCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Dpt. Biología Vegetal y EcologíaUniversidad de SevillaSevilleSpain
  2. 2.Instituto Multidisciplinario de Biología VegetalUniversidad Nacional de CórdobaCórdobaArgentina

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