Adaptational significance of variations in DNA methylation in clonal plant Hierochloe glabra (Poaceae) in heterogeneous habitats
Rujin Bian A , Dandan Nie A B , Fu Xing A D , Xiaoling Zhou A , Ying Gao A , Zhenjian Bai A and Bao Liu C
+ Author Affiliations
- Author Affiliations
A Institute of Grassland Science, Key Laboratory of Vegetation Ecology, Ministry of Education, Northeast Normal University, Changchun 130024, China.
B Hunchun Entry–Exit Inspection and Quarantine Bureau, Export Processing Zone, Hunchun 133300, China.
C Key Laboratory of Molecular Epigenetics of Ministry of Education and Institute of Genetics & Cytology, Northeast Normal University, Changchun 130024, China.
D Corresponding author. Email: xingf522@126.com
Australian Journal of Botany 61(4) 274-282 https://doi.org/10.1071/BT12242
Submitted: 23 June 2012 Accepted: 10 April 2013 Published: 24 May 2013
Abstract
As a prominent epigenetic modification, cytosine methylation may play a critical role in the adaptation of plants to different environments. The present study sought to investigate possible impacts of differential levels of nitrogen (N) supply on cytosine-methylation levels of a clonal plant, Hierochloe glabra Trin. (Poaceae). For this purpose, nitrate was applied at concentrations of 0, 0.15, 0.30 and 0.45 g N kg–1 soil, and ecologically important morphological traits were measured. The methylation-sensitive amplification polymorphism method was also conducted to analyse the variations in DNA cytosine methylation. Our results showed that N addition reduced CHG cytosine-methylation levels markedly compared with control plants growing in homogeneous pots (P = 0.026). No substantial differences were observed in morphological traits at the end of the growing stage, except for the highest ratio of leaf area to leaf dry mass in the medium-N patch (P = 0.008). However, significant linear regression relationships were found between cytosine-methylation levels and morphological traits, such as bud number and rhizome length and biomass. In conclusion, the higher cytosine-methylation level may activate asexual reproduction to produce more offspring and expand plant populations, possibly helping clonal plants to adapt to heterogeneous habitats.
Additional keywords: epigenetic variation, methylation-sensitive amplified polymorphism (MSAP), nutrient heterogeneity, phenotypic plasticity.
References
Aina R, Sgorbati S, Santagostino A, Labra M, Ghiani A, Citterio S (2004) Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiologia Plantarum 121, 472–480.| Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFOitbY%3D&md5=f0dc04fc9aad54ff8ed6ca1898d8d18cCAS |
Alpert P, Mooney HA (1986) Resource sharing among ramets in the clonal herb Fragaria chiloensis. Oecologia 70, 227–233.
| Resource sharing among ramets in the clonal herb Fragaria chiloensis.Crossref | GoogleScholarGoogle Scholar |
Ashikawa I (2001) Surveying CpG methylation at 5′-CCGG in the genomes of rice cultivars. Plant Molecular Biology 45, 31–39.
| Surveying CpG methylation at 5′-CCGG in the genomes of rice cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhvVeku78%3D&md5=80486979e6efe373c3b2b93679d9e78fCAS | 11247604PubMed |
Bai WM, Sun XQ, Wang ZW, Li LH (2009) Nitrogen addition and rhizome severing modify clonal growth and reproductive modes of Leymus chinensis population. Plant Ecology 205, 13–21.
| Nitrogen addition and rhizome severing modify clonal growth and reproductive modes of Leymus chinensis population.Crossref | GoogleScholarGoogle Scholar |
Bossdorf O, Arcuri D, Richards CL, Pigliucci M (2010) Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana. Evolutionary Ecology 24, 541–553.
| Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Boyko A, Kovalchuk I (2011) Genome instability and epigenetic modification: heritable responses to environmental stress? Current Opinion in Plant Biology 14, 260–266.
| Genome instability and epigenetic modification: heritable responses to environmental stress?Crossref | GoogleScholarGoogle Scholar | 21440490PubMed |
Bremner JM, Mulvaney CS (1982) Nitrogen-total. In ‘Methods of soil analysis’. (Eds AL Page, RH Miller, DR Keeney) pp. 595–608. (American Society of Agronomy: Madison, WI)
Burn JE, Bagnall DJ, Metzger JD, Dennis ES, Peacock WJ (1993) DNA methylation, vernalization, and the initiation of flowering. Proceedings of the National Academy of Sciences, USA 90, 287–291.
| DNA methylation, vernalization, and the initiation of flowering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhsVemu74%3D&md5=879e34038610be454ef0d08c50c4cb50CAS |
Cervera MT, Ruiz-Garcia L, Martinez-Zapater JM (2002) Analysis of DNA methylation in Arabidopsis thaliana based on methylation-sensitive AFLP markers. Molecular Genetics and Genomics 268, 543–552.
| Analysis of DNA methylation in Arabidopsis thaliana based on methylation-sensitive AFLP markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XptlWluro%3D&md5=8420425c0520a7f802f3dcd76a9e1444CAS | 12471452PubMed |
Choi CS, Sano H (2007) Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase- like protein in tobacco plants. Molecular Genetics and Genomics 277, 589–600.
| Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase- like protein in tobacco plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksVarsbw%3D&md5=dc30157fd7ef1909a48754e898766071CAS | 17273870PubMed |
Day KJ, John EA, Hutchings MJ (2003) The effects of spatially heterogeneous nutrient supply on yield, intensity of competition and root placement patterns in Briza media and Festuca ovina. Functional Ecology 17, 454–463.
| The effects of spatially heterogeneous nutrient supply on yield, intensity of competition and root placement patterns in Briza media and Festuca ovina.Crossref | GoogleScholarGoogle Scholar |
Dong M (1996) Clonal growth in plants in relation to resource heterogeneity: foraging behavior. Acta Botanica Sinica 38, 828–835.
Drake M, Colby WG, Bredakis E (1963) Yield of orchard grass as influenced by rates of nitrogen and harvest management. Agronomy Journal 55, 361–362.
| Yield of orchard grass as influenced by rates of nitrogen and harvest management.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXkslOku78%3D&md5=f923fc6b3e7ca997fbeeb6b7ff71b9b7CAS |
Fang JG, Chao CT (2007) Methylation-sensitive amplification polymorphism in date palms (Phoenix dactylifera L.) and their off-shoots. Plant Biology 9, 526–533.
| Methylation-sensitive amplification polymorphism in date palms (Phoenix dactylifera L.) and their off-shoots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVems7jO&md5=be58d94654be217dfe0f71406a922c31CAS | 17642034PubMed |
Farley RA, Fitter AH (1999) Temporal and spatial variation in soil resources in deciduous woodland. Journal of Ecology 87, 688–696.
| Temporal and spatial variation in soil resources in deciduous woodland.Crossref | GoogleScholarGoogle Scholar |
Finnegan EJ, Peacock WJ, Dennis ES (1996) Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proceedings of the National Academy of Sciences, USA 93, 8449–8454.
| Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkvFyksLg%3D&md5=14468ca8565b79cf77589d59a76ac4f3CAS |
Gao Y, Wang DL, Ba L, Bai YG, Liu B (2008) Interactions between herbivory and resource availability on grazing tolerance of Leymus chinensis. Environmental and Experimental Botany 63, 113–122.
| Interactions between herbivory and resource availability on grazing tolerance of Leymus chinensis.Crossref | GoogleScholarGoogle Scholar |
Gao Y, Xing F, Jin YJ, Nie DD, Wang Y (2012) Foraging responses of clonal plants to multi-patch environmental heterogeneity: spatial preference and temporal reversibility. Plant and Soil 359, 137–147.
| Foraging responses of clonal plants to multi-patch environmental heterogeneity: spatial preference and temporal reversibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlGmsr%2FO&md5=8ffff8bb8863c2fd8c9f005f12fb11a0CAS |
Gower ST, Kucharik CJ, Norman JM (1999) Direct and indirect estimation of leaf area index, f APAR, and net primary production of terrestrial ecosystems. Remote Sensing of Environment 70, 29–51.
| Direct and indirect estimation of leaf area index, f APAR, and net primary production of terrestrial ecosystems.Crossref | GoogleScholarGoogle Scholar |
Grativol C, Hemerly AS, Ferreira PCG (2012) Genetic and epigenetic regulation of stress responses in natural plant populations. Biochimicaet Biophysica Acta 1819, 176–185.
| Genetic and epigenetic regulation of stress responses in natural plant populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVWrs7o%3D&md5=f614b1c81f050b6766c12be23cb31966CAS |
Herrera CM, Bazaga P (2009) Quantifying the genetic component of phenotypic variation in unpedigreed wild plants: tailoring genomic scan for within-population use. Molecular Ecology 18, 2602–2614.
| Quantifying the genetic component of phenotypic variation in unpedigreed wild plants: tailoring genomic scan for within-population use.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptVaktbw%3D&md5=bb8b44e37d12aece997000bc6b7a0f2eCAS | 19457184PubMed |
Hilbricht T, Varotto S, Sgaramella V, Bartels D, Salamini F, Furini A (2008) Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection of the plant Craterostigma plantagineum. New Phytologist 179, 877–887.
| Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection of the plant Craterostigma plantagineum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVKns7vK&md5=8d8637cc4254763df7492f0cb4e51b05CAS | 18482228PubMed |
Hobolth A, Nielsen R, Wang Y, Wu FN, Steven DT (2006) CpG + CpNpG analysis of protein-coding sequences from tomato. Molecular Biology and Evolution 23, 1318–1323.
| CpG + CpNpG analysis of protein-coding sequences from tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlsVGqu70%3D&md5=174f280d708ddcf4c0cd5730621c2db2CAS | 16600999PubMed |
Hodge A (2006) Plastic plants and patchy soils. Journal of Experimental Botany 57, 401–411.
| Plastic plants and patchy soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKgsw%3D%3D&md5=9df42ac10a6fbe04e284c80f149f68e3CAS | 16172138PubMed |
Hutchings MJ, de Kroon H (1994) Foraging in plants: the role of morphological plasticity in resource acquisition. Advances in Ecological Research 25, 159–238.
| Foraging in plants: the role of morphological plasticity in resource acquisition.Crossref | GoogleScholarGoogle Scholar |
Hutchings MJ, Wijesinghe DK (1997) Patchy habitats, division of labour and growth dividends in clonal plants. Trends in Ecology & Evolution 12, 390–394.
| Patchy habitats, division of labour and growth dividends in clonal plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFOntw%3D%3D&md5=687aa4cd4bb57036954c2e0c3f03565fCAS |
Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. The Quarterly Review of Biology 84, 131–176.
| Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution.Crossref | GoogleScholarGoogle Scholar | 19606595PubMed |
Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski A, Albuisson J, Heredia F, Audigier P, Bouchez D, Dillmann C, Guerche P, Hospital F, Colot V (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLOS Genetics 5, e1000530
| Assessing the impact of transgenerational epigenetic variation on complex traits.Crossref | GoogleScholarGoogle Scholar | 19557164PubMed |
Kakutani T (2002) Epi-alleles in plants: Inheritance of epigenetic information over generations. Plant & Cell Physiology 43, 1106–1111.
| Epi-alleles in plants: Inheritance of epigenetic information over generations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xot12htLo%3D&md5=f75805648b5d54a11a0eb4f514275cbdCAS |
Kalisz S, Purugganan MD (2004) Epialleles via DNA methylation: consequences for plant evolution. Trends in Ecology & Evolution 19, 309–314.
| Epialleles via DNA methylation: consequences for plant evolution.Crossref | GoogleScholarGoogle Scholar |
Kidwell KK, Osborn TC (1992) Simple plant DNA isolation procedures. In ‘Plant genomes: methods for genetic and physical mapping’. (Eds JS Beckman, TC Osborn) pp. 1–13. (Kluwer Academic Publishers: Dordrecht, The Netherlands)
Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annual Review of Ecology and Systematics 27, 237–277.
| Evolutionary significance of local genetic differentiation in plants.Crossref | GoogleScholarGoogle Scholar |
Lira-Medeiros CF, Parisod C, Fernandes RA, Mata CS, Cardoso MA, Ferreira PCG (2010) Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS One 5, e10326
| Epigenetic variation in mangrove plants occurring in contrasting natural environment.Crossref | GoogleScholarGoogle Scholar | 20436669PubMed |
Marfil CF, Camadro EL, Masuelli RW (2009) Phenotypic instability and epigenetic variability in a diploid potato of hybrid origin, Solanum ruiz-lealii. BMC Plant Biology 9, 21
| Phenotypic instability and epigenetic variability in a diploid potato of hybrid origin, Solanum ruiz-lealii.Crossref | GoogleScholarGoogle Scholar | 19232108PubMed |
McClelland M, Nelson M, Raschke E (1994) Effect of site-specific modification on restriction endonucleases and DNA modification methyltransferases. Nucleic Acids Research 22, 3640–3659.
| Effect of site-specific modification on restriction endonucleases and DNA modification methyltransferases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmslejurk%3D&md5=35da59c7edc8ea0d3f72b76dd0e56ffbCAS | 7937074PubMed |
Mirouze M, Paszkowski J (2011) Epigenetic contribution to stress adaptation in plants. Current Opinion in Plant Biology 14, 267–274.
| Epigenetic contribution to stress adaptation in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnt1KmsLw%3D&md5=75a6a6ec23bc8eb8e5440392793e602cCAS | 21450514PubMed |
Monteuuis O, Doulbeau S, Verdeil JL (2008) DNA methylation in different origin clonal offspring from a mature Sequoiadendron giganteum genotype. Trees 22, 779–784.
| DNA methylation in different origin clonal offspring from a mature Sequoiadendron giganteum genotype.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlGhtLnP&md5=07caa9711a09a9f68e359f076c1f44afCAS |
Ni J, Zhang XS (2000) Climate variability, ecological gradient and the Northeast China Transect (NECT). Journal of Arid Environments 46, 313–325.
| Climate variability, ecological gradient and the Northeast China Transect (NECT).Crossref | GoogleScholarGoogle Scholar |
Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends in Ecology & Evolution 20, 481–486.
| Evolution of phenotypic plasticity: where are we going now?Crossref | GoogleScholarGoogle Scholar |
Portis E, Acqnadro A, Comino C, Lanteri S (2004) Analysis of DNA methylation during germination of pepper (Capsicum annuum L.) seeds using methylation-sensitive amplification polymorphism (MSAP). Plant Science 166, 169–178.
| Analysis of DNA methylation during germination of pepper (Capsicum annuum L.) seeds using methylation-sensitive amplification polymorphism (MSAP).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltVyisg%3D%3D&md5=9ccaec16482ca934fdf8e3ac9864b84dCAS |
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. Molecular & General Genetics 253, 703–710.
| Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms.Crossref | GoogleScholarGoogle Scholar |
Richards EJ (2011) Natural epigenetic variation in plant species: a view from the field. Current Opinion in Plant Biology 14, 204–209.
| Natural epigenetic variation in plant species: a view from the field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltFyrtr4%3D&md5=1d22fffe72d61b27366041b8260a44cdCAS | 21478048PubMed |
Rohlf FJ (2000) ‘NTSYS-pc: numerical taxonomy and multivariate analysis system, version 2.10e.’(Exeter Publications: New York)
Roiloa SR, Retuerto R (2006) Small-scale heterogeneity in soil quality influences photosynthetic efficiency and habitat selection in a clonal plant. Annals of Botany 98, 1043–1052.
| Small-scale heterogeneity in soil quality influences photosynthetic efficiency and habitat selection in a clonal plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlantbbE&md5=ce45072cbe30c10e5648d4189d844ab0CAS | 16987921PubMed |
Scheepens JF, Frei ES, Stocklin J (2010) Genotypic and environmental variation in specific leaf area in a widespread Alpine plant after transplantation to different altitudes. Oecologia 164, 141–150.
| Genotypic and environmental variation in specific leaf area in a widespread Alpine plant after transplantation to different altitudes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cjks1yltQ%3D%3D&md5=8fe7dfe60259b1e07e67d188ccec4540CAS | 20461412PubMed |
Sherman JD, Talbert LE (2002) Vernalization-induced changes of the DNA methylation pattern in winter wheat. Genome 45, 253–260.
| Vernalization-induced changes of the DNA methylation pattern in winter wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtlSns7k%3D&md5=735bb67e8593783266047866b1879d9fCAS | 11962622PubMed |
Steward N, Ito M, Yamaguchi Y, Koizumi N, Sano H (2002) Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress. The Journal of Biological Chemistry 277, 37 741–37 746.
| Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVejtrk%3D&md5=ea0457e3a4f9fb5865eee612e2f4309dCAS |
Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A (2010a) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytologist 185, 1108–1118.
| Stress-induced DNA methylation changes and their heritability in asexual dandelions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksFCrt7c%3D&md5=f8eab0ae0df148ac327c06c27c564791CAS |
Verhoeven KJF, van Dijk PJ, Biere A (2010b) Changes in genomic methylation patterns during the formation of triploid asexual dandelion lineages. Molecular Ecology 19, 315–324.
| Changes in genomic methylation patterns during the formation of triploid asexual dandelion lineages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlOntLo%3D&md5=f2679642a0884a29d7338733606dbf5dCAS |
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science 37, 29–38.
| An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaA2cXitlGmug%3D%3D&md5=370a7f1ec56474a96c9131c5cba6ec91CAS |
Wang D, Ba L (2008) Ecology of meadow steppe in northeast China. The Rangeland Journal 30, 247–254.
| Ecology of meadow steppe in northeast China.Crossref | GoogleScholarGoogle Scholar |
Wang ZW, Xu AK, Zhu TC (2008) Plasticity in bud demography of a rhizomatous clonal plant Leymus chinensis L. in response to soil water status. Journal of Plant Biology 51, 102–107.
| Plasticity in bud demography of a rhizomatous clonal plant Leymus chinensis L. in response to soil water status.Crossref | GoogleScholarGoogle Scholar |
Wang WS, Zhao XQ, Pan YJ, Zhu LH, Fu BY, Li ZK (2011) DNA methylation changes detected by methylation-sensitive amplified polymorphism in two contrasting rice genotypes under salt stress. Journal of Genetics and Genomics = Yi Chuan Xue Bao 38, 419–424.
| DNA methylation changes detected by methylation-sensitive amplified polymorphism in two contrasting rice genotypes under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlOmsLrN&md5=a0163f2b4569a1c6bb075ec7d6746afaCAS |
Welham CVJ, Turkington R, Sayre C (2002) Morphological plasticity of white clover (Trifolium repens L.) in response to spatial and temporal resource heterogeneity. Oecologia 130, 231–238.
Xiong LZ, Xu GC, Saghai-Maroof MA, Zhang Q (1999) Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Molecular & General Genetics 261, 439–446.
| Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsFChtL0%3D&md5=c702f820a16f510305b668158253c457CAS |
Zhang YY, Fischer M, Colot V, Bossdorf O (2013) Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytologist 197, 314–322.
| Epigenetic variation creates potential for evolution of plant phenotypic plasticity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslelsL7I&md5=5c9ce5e9907eaaa19e922faf6733da64CAS | 23121242PubMed |
