Skip to main content
SpringerLink
Log in

Meiotic Pairing Inadequacies at the Levels of X Chromosome, Gene, or Base: Epigenetic Tagging for Transgenerational Error-Correction Guided by a Future Homologous Duplex

  • Original Article
  • Published:
Biological Theory Aims and scope Submit manuscript

Abstract

In contrast to the two X chromosomes that participate equally in oogenic meiosis in mammals, during spermatogenesis the solitary X chromosome can be regarded as an inadequate pairing partner for the Y chromosome. Hence it is epigenetically silenced and consigned to the XY body. This silenced state can transfer between generations. The sleeping X will awake when in a female cell with an accompanying maternally donated X chromosome (a homologous DNA duplex). Transgene experiments in nematodes indicate that a similar process can operate at the level of chromosomal segments. A gene that mispairs at meiosis is epigenetically silenced and transferred to the next generation where its awakening is conditional on the presence of a meiotic pairing partner. These intergenerational transfers of epigenetic labelling, and intragenerational reversals thereof, might apply at the level of individual bases when confronted with inadequate pairing partners. During meiotic recombination, homologous DNA sequences of maternal and paternal origin pair to form a mutual duplex, and mismatches can be detected and corrected (gene conversion). But there is only a 50 % chance that the correction will favor a particular allele. There is information that a DNA duplex segment is in need of correction, but not how correction could asymmetrically favor one allele (generally the wild-type). If the segment were epigenetically marked as “suspect,” this information could be used in a future generation to favorably correct should more information, in the form of a homologous unmutated duplex, became available. So fundamental would this mechanism be that it would have provided a selection pressure for the emergence of epigenetic marking early in evolution.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arbeithuber B, Betancourt AJ, Ebner T, Tiemann-Boege I (2015) Crossovers are associated with mutation and biased gene conversion at recombination hotspots. Proc Natl Acad Sci USA 112:2109–2114

    Article  Google Scholar 

  • Baarends WM, Wassenaar E, van der Laan R et al (2005) Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis. Mol Cell Biol 25:1041–1053

    Article  Google Scholar 

  • Baker CL, Shimpei Kajita S, Walker M et al (2015) PRDM9 drives evolutionary erosion of hotspots in Mus musculus through haplotype-specific initiation of meiotic recombination. PLoS Genet 11:e1004916

    Article  Google Scholar 

  • Bateson W, Pellew C (1915) On the genetics of ‘rogues’ among culinary peas (Pisum sativum). J Genet 5:15–36

    Article  Google Scholar 

  • Battail G (2014) Information and life. Springer, Dordrecht

    Book  Google Scholar 

  • Bean CJ, Schaner CE, Kelly WG (2004) Meiotic pairing and imprinted X chromatin assembly in Caenorhabditis elegans. Nature Genet 36:100–105

    Article  Google Scholar 

  • Bengtsson BO (1986) Biased conversion as the primary function of recombination. Genet Res 47:77–80

    Article  Google Scholar 

  • Bhattacharyya T, Gregorova S, Mihola O et al (2013) Mechanistic basis of infertility of mouse intersubspecific hybrids. Proc Natl Acad Sci USA 110:E468–E477

    Article  Google Scholar 

  • Brand CL, Presgraves DC (2016) Evolution: on the origin of symmetry, synapsis, and species. Curr Biol 26:R319–R337

    Article  Google Scholar 

  • Brink RA (1956) A genetic change associated with the R Locus in maize which is directed and potentially reversible. Genetics 41:872–889

    Google Scholar 

  • Butler S (1878) Life and habit. Trübner, London

    Google Scholar 

  • Butler S (1926) In: Jones HF, Bartholomew AT (eds) The Shrewbury edition of the works of Samuel Butler, vol 20. Cape, London, p 13

    Google Scholar 

  • Bygren LO, Tinghög P, Cartensen J et al (2014) Change in paternal grandmothers’ early food supply influenced cardiovascular mortality of female grandchildren. BMC Genet 15:12

    Article  Google Scholar 

  • Cooper DW (1971) Directed genetic change model for X chromosome inactivation in eutherian mammals. Nature 230:292–294

    Article  Google Scholar 

  • Davies B et al (2016) Re-engineering the zinc fingers of PRDM9 reverses hybrid sterility in mice. Nature 530:171–176

    Article  Google Scholar 

  • Engel N (2015) Imprinted X chromosome inactivation offers up a double dose of epigenetics. Proc Natl Acad Sci USA 112:14408–14409

    Article  Google Scholar 

  • Forsdyke DR (1981) Are introns in-series error detecting sequences? J Theor Biol 93:861–866

    Article  Google Scholar 

  • Forsdyke DR (1994) Relationship of X chromosome dosage compensation to intracellular self/not-self discrimination: a resolution of Muller’s paradox? J Theor Biol 167:7–12

    Article  Google Scholar 

  • Forsdyke DR (1995) Entropy-driven protein self-aggregation as the basis for self/not-self discrimination in the crowded cytosol. J Biol Syst 3:273–287

    Article  Google Scholar 

  • Forsdyke DR (1996) Different biological species “broadcast” their DNAs at different (G+C)% “wavelengths.” J Theor Biol 178:405–417

    Article  Google Scholar 

  • Forsdyke DR (2001) The origin of species revisited. A victorian who anticipated modern developments in darwin’s theory. McGill-Queen’s University Press, Montreal

    Google Scholar 

  • Forsdyke DR (2009) X chromosome reactivation perturbs intracellular self/not-self discrimination. Immun Cell Biol 87:525–528

    Article  Google Scholar 

  • Forsdyke DR (2011) The selfish gene revisited. Biol Theor 5:246–255

    Article  Google Scholar 

  • Forsdyke DR (2012) Ohno’s hypothesis and muller’s paradox: sex chromosome dosage compensation may serve collective gene functions. BioEssays 34:930–933

    Article  Google Scholar 

  • Forsdyke DR (2013) Introns first. Biol Theor 7:196–203

    Article  Google Scholar 

  • Forsdyke DR (2016) Evolutionary bioinformatics, 3rd edn. Springer, New York

    Book  Google Scholar 

  • Gartler SM (2014) A brief history of dosage compensation. J Genet 93:591–595

    Article  Google Scholar 

  • Gavrilov LA, Gavrilova NS, Kroutko VN et al (1997) Mutation load and human longevity. Mut Res 377:61–62

    Article  Google Scholar 

  • Gladyshev E, Kleckner N (2014) Direct recognition of homology between double helices of DNA in Neurospora crassa. Nature Comm 5:3509

    Article  Google Scholar 

  • Gould SJ (1993) Fulfilling the spandrels of world and mind. In: Selzer J (ed) Understanding scientific prose. University of Wisconsin Press, Madison, pp 310–336

    Google Scholar 

  • Graves JAM (1996) Mammals that break the rules: genetics of marsupials and monotremes. Annu Rev Genet 30:233–260

    Article  Google Scholar 

  • Hamming RW (1980) Coding and information theory. Prentice-Hall, Englewood Cliffs

    Google Scholar 

  • Hare JT, Taylor JH (1985) One role for DNA methylation in vertebrate cells is strand discrimination in mismatch repair. Proc Natl Acad Sci USA 82:7350–7354

    Article  Google Scholar 

  • Huynh KD, Lee JT (2004) A continuity of X-chromosome silence from gamete to zygote. Cold Spring Harb Q Biol 69:103–112

    Article  Google Scholar 

  • Leopold LE, Heestand BN, Seonga S et al (2015) Lack of pairing during meiosis triggers multigenerational transgene silencing in Caenorhabditis elegans. Proc Natl Acad Sci USA 112:E2667–E2676

    Article  Google Scholar 

  • Liao D (1999) Concerted evolution, molecular mechanism and biological implications. Am J Hum Genet 64:24–30

    Article  Google Scholar 

  • Lifschytz E, Lindsley DL (1972) The role of X-chromosome inactivation during spermatogenesis. Proc Natl Acad Sci USA 69:182–186

    Article  Google Scholar 

  • Lyon MF (1961) Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190:372–373

    Article  Google Scholar 

  • Lyon MF (1999) Imprinting and X chromosome inactivation. In: Ohlsson R (ed) Results and problems in cell differentiation. Springer, Heidelberg, pp 73–90

    Google Scholar 

  • Makova KD, Li W-H (2002) Strong male-driven evolution of DNA sequences in humans and apes. Nature 416:624–626

    Article  Google Scholar 

  • Marcet-Houben M, Gabaldón T (2015) Beyond the whole-genome duplication: phylogenetic evidence for an ancient interspecies hybridization in the baker’s yeast lineage. PLoS Biol 13:e1002220

    Article  Google Scholar 

  • McKee BD (1996) Meiotic recombination: a mechanism for tracking and eliminating mutations? BioEssays 18:411–419

    Article  Google Scholar 

  • Miklos GLG (1974) Sex-chromosome pairing and male fertility. Cytogenet Cell Genet 13:558–577

    Article  Google Scholar 

  • Muller HJ (1950) Evidence of the precision of genetic adaptation. Harvey Lect 43:165–229

    Google Scholar 

  • Palamara PF, Francioli LC, Wilton PR et al (2015) Leveraging distant relatedness to quantify human mutation and gene-conversion rates. Am J Hum Genet 97:775–789

    Article  Google Scholar 

  • Pembrey ME, Bygren LO, Kaati G et al (2006) Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet 14:159–166

    Article  Google Scholar 

  • Reanney DC (1979) RNA splicing and polynucleotide evolution. Nature 277:598–600

    Google Scholar 

  • Reanney DC (1984) RNA splicing as an error-screening mechanism. J Theor Biol 110:315–321

    Article  Google Scholar 

  • Reese V (2002) Mutation repair: a proposed mechanism that would enable complex genomes to better resist mutational entropy and which suggests a novel function for meiosis. In: The human behavior and evolution society 14th annual meeting, Rutgers University. Abstracts of presentations to session on “New Developments in Biology,” June 21, p 40

  • Rozen S, Skaletsky H, Marszalek JD et al (2003) Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 423:873–876

    Article  Google Scholar 

  • Schaefer S, Nadeau JH (2015) The genetics of epigenetic inheritance: modes, molecules, and mechanisms. Quart Rev Biol 90:381–415

    Article  Google Scholar 

  • Shiu PK, Raju NB, Zickler D, Metzenberg RL (2001) Meiotic silencing by unpaired DNA. Cell 107:905–916

    Article  Google Scholar 

  • Speed RM (1986) Oocyte development in XO foetuses of man and mouse: the possible role of heterologous X-chromosome pairing in germ cell survival. Chromosoma 94:115–124

    Article  Google Scholar 

  • Sun S, Payer B, Namekawa S et al (2015) Xist imprinting is promoted by the hemizygous (unpaired) state in the male germ line. Proc Natl Acad Sci USA 112:14415–14422

    Article  Google Scholar 

  • Turner JMA (2015) Meiotic silencing in mammals. Annu Rev Genet 49:395–412

    Article  Google Scholar 

  • Turner JMA, Mahadevaiah SK, Fernandez-Capetillo O et al (2005) Silencing of unsynapsed meiotic chromosomes in the mouse. Nature Genet 37:41–47

    Google Scholar 

  • Wahls WP, Davidson MK (2011) DNA sequence-mediated, evolutionarily rapid redistribution of meiotic recombination hotspots. Genetics 189:685–694

    Article  Google Scholar 

  • Wahls WP, Davidson MK (2012) New paradigms for conserved, multifactorial, cis-acting regulation of meiotic recombination. Nucelic Acids Res 40:9983–9989

    Article  Google Scholar 

  • Wang J, Syrett CM, Kramer MC et al (2016) Unusual maintenance of X chromosome inactivation predisposes female lymphocytes for increased expression from the inactive X. Proc Natl Acad Sci USA 113:E2029–E2038

    Article  Google Scholar 

  • Winge Ő (1917) The chromosomes. Their numbers and general importance. Compt Rendus Trav Lab Carlsberg 13:131–275

    Google Scholar 

  • Yang S, Yuan Y, Wang L et al (2012) Great majority of recombination events in Arabidopsis are gene conversion events. Proc Natl Acad Sci USA 109:20992–20997

    Article  Google Scholar 

  • Zhao J, Sun BK, Erwin JA et al (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322:750–756

    Article  Google Scholar 

Download references

Acknowledgments

Queen’s University hosts Forsdyke’s webpages, where copies of some of the references may be found.

Author information

Authors and Affiliations

  1. Independent Scholar, Bartlesville, OK, USA

    Virgil R. Reese

  2. Department of Biomedical and Molecular Sciences, Queen’s University, Kingston, ON, Canada

    Donald R. Forsdyke

Authors
  1. Virgil R. Reese
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Donald R. Forsdyke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Donald R. Forsdyke.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Reese, V.R., Forsdyke, D.R. Meiotic Pairing Inadequacies at the Levels of X Chromosome, Gene, or Base: Epigenetic Tagging for Transgenerational Error-Correction Guided by a Future Homologous Duplex. Biol Theory 11, 150–157 (2016). https://doi.org/10.1007/s13752-016-0242-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13752-016-0242-6

Keywords

Search

Navigation