Polyploidy and transposons

Abstract

In his interesting commentary on transposable elements (TEs), gene silencing and macroevolution, John McDonald[1xMcDonald, J. Trends Ecol. Evol. 1998; 13: 94–95Abstract | Full Text PDF | PubMed | Scopus (52)See all References[1]omitted a major player that has acted in concert with TEs to drive vertebrate and plant evolution, namely, polyploidy. The quantum increases in gene number that are correlated with landmark evolutionary events have often resulted from whole-genome duplications. The transition from invertebrates to jawed vertebrates involved two rounds of polyploidization[2xSpring, J. FEBS Lett. 1997; 400: 2–8Abstract | Full Text | Full Text PDF | PubMed | Scopus (208)See all References[2]. An estimated 70% of flowering plant species have polyploidy in their history[3xMasterson, J. Science. 1994; 264: 421–424Crossref | PubMedSee all References[3].Polyploidy permits extensive genome modification by TEs because, unlike diploid genomes (which are susceptible to insertional mutagenesis), polyploid genomes contain duplicates of all genes and, consequently, are relatively well buffered from the deleterious consequences of transposition[4xMatzke, M.A. and Matzke, A.J.M. Novartis Found. Symp. 1998; 214: 168–186PubMedSee all References[4]. Transposable elements will therefore tend to multiply and be maintained in polyploid genomes, because extra copies of genes compensate for losses or alterations in expression incurred through TE insertions. With respect to gene silencing, if it is assumed that TEs are the primary targets of epigenetic modifications, such as methylation[5xYoder, J.A., Walsh, C.P., and Bestor, T.H. Trends Genet. 1997; 13: 335–339Abstract | Full Text PDF | PubMed | Scopus (1221)See all References[5], and that polyploids tolerate transposition, then it would follow that polyploid genomes contain more TEs and are more highly methylated than diploid genomes[4xMatzke, M.A. and Matzke, A.J.M. Novartis Found. Symp. 1998; 214: 168–186PubMedSee all References[4]. Indeed, a rough correlation exists: global methylation is found in vertebrate and polyploid plant genomes, which contain a high proportion of TEs, whereas fractional methylation is observed in some invertebrates and the diploid plant Arabidopsis thaliana (which has not accumulated significant numbers of TEs)[4xMatzke, M.A. and Matzke, A.J.M. Novartis Found. Symp. 1998; 214: 168–186PubMedSee all References, 6xTweedie, S. et al. Mol. Biol. Cell. 1997; 17: 1469–1475See all References].Of course, factors in addition to polyploidy, such as the insertion-site preferences of different TEs, can also influence the distribution and abundance of TEs in genomes. For example, an element that preferentially integrates copies of itself, such as Tdd-1 in the slime mould Dictyostelium discoideum[7xSandmeyer, S., Hansen, L., and Chalker, D. Annu. Rev. Genet. 1990; 24: 491–518Crossref | PubMedSee all References[7], could potentially attain a high copy number in a diploid genome. Instead of epigenetic silencing systems having originated to accommodate increases in gene number[8xBird, A.P. Trends Genet. 1995; 11: 94–100Abstract | Full Text PDF | PubMed | Scopus (321)See all References[8], it is more likely that pre-existing defensive epigenetic modifications, targeted against TEs or viruses, were elaborated and became pervasive in polyploid genomes as TE populations expanded. The consequences would be the same as they are for vertebrates and many plants: an increased genomic methylation and apparent recruitment of a primordial genome defense (i.e. methylation) for regulating differential gene expression. These observations suggest that genes whose repression is correlated with methylation contain TEs or TE remnants in their promoters.Another point is that epigenetic silencing induced by transposable elements can have implications for evolution if meiotically heritable silencing occurs[9xSee all References[9]. We are only just beginning to understand the numerous ways in which TEs (and other sequences perceived as `foreign' by the genome defense system) can interact in cis- and in trans-associations, via DNA sequence identity, to induce gene silencing and epigenetic modifications[10xMatzke, M.A. and Matzke, A.J.M. Cell Mol. Life Sci. 1998; 54: 94–103Crossref | PubMed | Scopus (67)See all References, 11xMartienssen, R. Curr. Biol. 1996; 6: 810–813Abstract | Full Text | Full Text PDF | PubMed | Scopus (59)See all References]. In plants and, perhaps, other organisms, non-Mendelian inheritance can result from these interactions, because interacting alleles or loci exhibit altered expression after segregating in progeny. In some cases, epigenetic silencing induced by foreign sequences can persist and influence phenotypes for many sexual generations[10xMatzke, M.A. and Matzke, A.J.M. Cell Mol. Life Sci. 1998; 54: 94–103Crossref | PubMed | Scopus (67)See all References[10], and thus be indistinguishable from genetic mutations. In summary, the genetic and epigenetic consequences of transposition in polyploids are an important aspect of the creative power attributed to redundancy[12xSee all References[12].