Skip to main content

Advertisement

Log in

Epigenetic divergence of key genes associated with water temperature and salinity in a highly invasive model ascidian

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Invasive species offer good models for studying mechanisms of response to rapid changing environments in the wild. DNA methylation is considered to be one of crucial drivers for rapid local adaptation. However, the extent of epigenetic variation and the factors driving such variation remain largely unexplored in biological invasions. Here we used direct bisulfite sequencing to investigate DNA methylation patterns of five key genes corresponding to two important environmental factors in marine ecosystems, water temperature and salinity, in a model invasive ascidian Ciona robusta (=C. intestinalis spA). Our results clearly showed that DNA methylation mainly occurred in gene bodies, rather than promoters, at regions with low values of CpG O/E. We detected significant variation of DNA methylation among populations in two genes (heat shock protein 90 and Na+-K+-2Cl cotransporter). Interestingly, significant correlation was detected between methylation levels and the two environmental factors at some CpGs in these two genes. When the data of all CpGs was subjected to principal component analysis, individuals were assigned back to their population orgins. All the results suggest that environmental factors likely contribute, at least partially, to the observed DNA methylation variation. Such variation, either by some loci alone or through gene networks, might be involved in rapid local adaptation during biological invasions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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 19:1283–1295

    Article  CAS  PubMed  Google Scholar 

  • Bates WR (2005) Environmental factors affecting reproduction and development in ascidians and other Protochordates. Can J Zool 83:51–61

    Article  Google Scholar 

  • Bird AP (1980) DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res 8:1499–1504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunetti R et al (2015) Morphological evidence that the molecularly determined Ciona intestinalis type A and type B are different species: Ciona robusta and Ciona intestinalis. J Zoolog Syst Evol Res 53:186–193

    Article  Google Scholar 

  • Ciancio JE, Rossi CR, Pascual M, Anderson E, Garza JC (2015) The invasion of an Atlantic Ocean river basin in Patagonia by Chinook salmon: new insights from SNPs. Biol Invasions 17:2989–2998

    Article  Google Scholar 

  • Colautti RI, Lau JA (2015) Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Mol Ecol 24:1999–2017

    Article  PubMed  Google Scholar 

  • Dehal P et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167

    Article  CAS  PubMed  Google Scholar 

  • Dray S, Dufour A (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Article  Google Scholar 

  • Dyachenko OV et al (2006) Effect of hypermethylation of CCWGG sequences in DNA of Mesembryanthemum crystallinum plants on their adaptation to salt stress. Biochemistry (Mosc) 71:461–465

    Article  CAS  Google Scholar 

  • Elango N, Hunt BG, Goodisman MAD, Yi SV (2009) DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proc Natl Acad Sci U S A 106:11206–11211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177

    Article  CAS  PubMed  Google Scholar 

  • Feil R (2006) Environmental and nutritional effects on the epigenetic regulation of genes. Mutat Res 600:46–57

    Article  CAS  PubMed  Google Scholar 

  • Feng S et al (2010) Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci U S A 107:8689–8694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gamba G (2005) Molecular physiology and pathophysiology of electroneutral cation chloride cotransporters. Physiol Rev 85:423–493

    Article  CAS  PubMed  Google Scholar 

  • Gavery MR, Roberts SB (2010) DNA methylation patterns provide insight into epigenetic regulation in the Pacific oyster (Crassostrea gigas). BMC Genom 11:483

    Article  Google Scholar 

  • Glastad KM, Hunt BG, Goodisman MAD (2013) Evidence of aconserved functional role for DNA methylation intermites. Insect Mol Biol 22:143–154

    Article  CAS  PubMed  Google Scholar 

  • Han X, Patters AB, Jones DP, Zelikovic I, Chesney RW (2006) The taurine transporter: mechanisms of regulation. Acta Physiol (Oxf) 187:61–73

    Article  CAS  Google Scholar 

  • Hudson J, Viard F, Roby C, Rius M (2016) Anthropogenic transport of species across native ranges: unpredictable genetic and evolutionary consequences. Bio Lett 12:20160620

    Article  Google Scholar 

  • Jiang M et al (2010) Rapid quantification of DNA methylation by measuring relative peak heights in direct bisulfite-PCR sequencing traces. Lab Invest 90:282–290

    Article  CAS  PubMed  Google Scholar 

  • Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13:484–492

    Article  CAS  PubMed  Google Scholar 

  • Kass SU, Pruss D, Wolffe AP (1997) How does DNA methylation repress transcription? Trends Genet 13:444–449

    Article  CAS  PubMed  Google Scholar 

  • Kirkpatrick M, Barrett B (2015) Chromosome inversions, adaptive cassettes and the evolution of species’ ranges. Mol Ecol 24:2046–2055

    Article  PubMed  Google Scholar 

  • Kou HP et al (2011) Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice (Oryza sativa L.). J Plant Physiol 168:1685–1693

    Article  CAS  PubMed  Google Scholar 

  • Li LC, Dahiya R (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18:1427–1431

    Article  CAS  PubMed  Google Scholar 

  • Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC (2005) Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135:1382–1386

    CAS  PubMed  Google Scholar 

  • Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. CMLS Cell Mol Life Sci 62:670–684

    Article  CAS  PubMed  Google Scholar 

  • Mirouze M, Paszkowski J (2011) Epigenetic contribution to stress adaptation in plants. Curr Opin Plant Biol 14:267–274

    Article  CAS  PubMed  Google Scholar 

  • Nydam ML, Harrison RG (2010) Polymorphism and divergence within the ascidian genus Ciona. Mol Phylogenet Evol 56:718–726

    Article  PubMed  Google Scholar 

  • Pecinka A et al (2010) Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell 22:3118–3129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294

    Article  CAS  PubMed  Google Scholar 

  • Procaccini G, Affinito O, Toscano F, Sordino P (2011) A new animal model for merging ecology and evolution. In: Evolutionary biology–concepts, biodiversity, macroevolution and genome evolution. Springer, Berlin Heidelberg, pp 91–106

  • Richards EJ (2006) Inherited epigenetic variation—revisiting soft inheritance. Nat Rev Genet 7:395–401

    Article  CAS  PubMed  Google Scholar 

  • Rocha RM, Kremer LP, Baptista MS, Metri R (2009) Bivalve cultures provide habitat for exotic tunicates in southern Brazil. Aquat Invasions 4:195–205

    Article  Google Scholar 

  • Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Annu Rev Mar Sci 3:509–535

    Article  Google Scholar 

  • Sarda S, Zeng J, Hunt BG, Yi SV (2012) The evolution of invertebrate gene body methylation. Mol Biol Evol 29:1907–1916

    Article  CAS  PubMed  Google Scholar 

  • Sato A, Kawashima T, Fujie M, Hughes S, Satoh N, Shimeld SM (2015) Molecular basis of canalization in an ascidian species complex adapted to different thermal conditions. Scientific Reports 5:16717–16725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo KS, Lee Y (2009) A First Assessment of Invasive Marine Species on Chinese and Korean Coasts. Biological Invasions in Marine Ecosystems 204:577–585

    Article  Google Scholar 

  • Skou JC, Esmann M (1992) The Na+, K+-ATPase. J Bioenerg, Biomembrane 24:249–261

    CAS  Google Scholar 

  • Sumner S, Pereboom JM, Jordan WC (2006) Differential gene expression and phenotypic plasticity in behavioural castes of the primitively eusocial wasp, Polistes canadensis. Proceedings of the Royal Society B 273:19–26

    Article  CAS  PubMed  Google Scholar 

  • Suzuki MM, Kerr ARW, Sousa DD, Bird A (2007) CpG methylation is targeted to transcription units in an invertebrate genome. Genome Res 17:625–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takuno S, Gaut BS (2012) Body-methylated genes in Arabidopsis thaliana are functionally important and evolve slowly. Mol Biol Evol 29:219–227

    Article  CAS  PubMed  Google Scholar 

  • Tsai JR, Lin HC (2007) V-type H+-ATPase and Na+, K+-ATPase in the gills of 13 euryhaline crabs during salinity acclimation. J Exp Biol 210:620–627

    Article  CAS  PubMed  Google Scholar 

  • Vabulas RM, Raychaudhuri S, Hayer-Hartl M, Hartl FU (2010) Protein Folding in the Cytoplasm and the Heat Shock Response. Cold Spring Harb Perspect Biol 2:a004390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vinson JP et al (2005) Assembly of polymorphic genomes: algorithms and application to Ciona savignyi. Genome Res 15:1127–1135

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang X et al (2013) Function and evolution of DNA methylation in nasonia vitripennis. PLoS Genet 9:e1003872

    Article  PubMed  PubMed Central  Google Scholar 

  • Weaver ICG et al (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7:847–854

    Article  CAS  PubMed  Google Scholar 

  • Xiang H et al (2010) Single base resolution methylome of the silkworm reveals a sparse epigenomic map. Nat Biotechnol 28:516–520

    Article  CAS  PubMed  Google Scholar 

  • Xie HJ et al (2015) ICE1 demethylation drives the range expansion of a plant invader through cold tolerance divergence. Mol Ecol 24:835–850

    Article  CAS  PubMed  Google Scholar 

  • Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830

    Article  CAS  PubMed  Google Scholar 

  • Zemach A, McDaniel IE, Silva P, Zilberman D (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916–919

    Article  CAS  PubMed  Google Scholar 

  • Zhan A, MacIsaac HJ, Cristescu ME (2010) Invasion genetics of the Ciona intestinalis species complex: from regional endemism to global homogeneity. Mol Ecol 19:4678–4694

    Article  CAS  PubMed  Google Scholar 

  • Zhan A, Darling JA, Bock DG, Lacoursière-Rousse A, MacIsaac HJ, Cristescu ME (2012) Complex genetic patterns in closely related colonizing invasive species. Ecol Evol 2:1331–1346

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhan A, Briski E, Bock DG, Ghabooli S, MacIsaac HJ (2015) Ascidians as models for studying invasion success. Mar Biol 162:2449–2470

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31622011; 31272665) and 100-Talent Program of the Chinese Academy of Sciences to A.Z.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aibin Zhan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 2754 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pu, C., Zhan, A. Epigenetic divergence of key genes associated with water temperature and salinity in a highly invasive model ascidian. Biol Invasions 19, 2015–2028 (2017). https://doi.org/10.1007/s10530-017-1409-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-017-1409-1

Keywords

Navigation