18.8 Transposons

18.8 Transposons

Transposable elements (TE) are ubiquitous and vital components of almost all prokaryotic and eukaryotic genomes. Eukaryotic transposons are classified into two main classes:

  • Class I elements, also known as retrotransposons, use an RNA intermediate during transposition, which is transcribed from its DNA template; the reverse transcriptase which does this is often encoded by the TE itself.
  • Class II TEs form a large and diverse group of mobile elements, but the most important of these in fungi are those with a ‘cut-and-paste’ transposition mechanism that does not involve an RNA intermediate. These transpositions are catalysed by an endonuclease (transposase), which is encoded within the TE; the basic architecture of which comprises a transposase and terminal inverted repeats (TIRs), which are the excision sites for the transposase. The transposase makes a staggered cut at the excision sites producing sticky ends, cuts out the DNA transposon and ligates it into target sites elsewhere in the genome. Some transposases bind non-specifically to any target site in the DNA; others bind to specific target sequences. DNA polymerase fills in the single-strand gaps resulting from the sticky ends and DNA ligase closes the sugar-phosphate backbone. This results in excision site duplication and the insertion sites of DNA transposons can be identified by short direct repeats (resulting from the DNA polymerase repair of the staggered cut in the target DNA) followed by inverted repeats of the excision sites (required for any future TE excision by transposase).

Cut-and-paste TEs may be duplicated if their transposition takes place during S phase of the cell cycle while the DNA is being replicated and this can result in gene duplication, which plays an important role in genomic evolution.

Fungal genomes are exceptionally variable in their TE content, varying over the range 0.02 to 29.8% of their genome consisting of transposable elements, and like other eukaryotes, each fungal transposable element is either of class I or of class II. Here again, though, there is tremendous variability, with the genomes of two strains of Pleurotus ostreatus populated mainly by Class I elements.

A survey of 1,730 fungal genomes for transposable elements found DNA TEs across the whole data set but with an uneven distribution in terms of both TE classification and fungal classification. TE content generally correlated with genome size, and TE count is associated with the lifestyle, being elevated in mycorrhizas and diminished in animal parasites.

Interestingly, TEs are opposed by several genome defence mechanisms including Repeat-Induced Point mutation (RIP) and RNA interference (where RNA molecules inhibit gene expression or translation, by neutralizing targeted mRNA molecules; now called RNAi, but also known as co-suppression, post-transcriptional gene silencing and quelling).

Fungi that possessed RIP and RNAi systems had more total TE sequences but fewer elements retaining a functional transposase. This indicates stringent control over transposition and an expression of epigenetic defence intended to suppress TE expression and limit their proliferation (Gladyshev, 2017).

 There are very few DNA transposons in genomes belonging to the oldest fungal lineages; the Cryptomycota, Microsporidia, Chytridiomycota, and Blastocladiomycota. Lower terrestrial fungi vary in their TE composition: Glomeromycotina have large genomes with more than 80,000 copies of DNA TEs, but only 59 have been found in Mortierella alpina (though this genome had about 4,000 remnant copies, that lacked transposase) and 165 in Mortierella elongata.

Genome architectures of Ascomycota also varied significantly. Most members of Saccharomycetes had fewer than 20 TE copies with a transposase domain whereas species of Erysiphe, Tuber, and Pseudogymnoascus could have thousands of DNA TEs.

Among Basidiomycota, two contrasting genome architectures have been distinguished: those with compact genomes with only a handful of transposons (Ustilaginomycotina, Microbotryomycetes) and those with large genomes with a very large number of transposons, e.g. Agaricomycetes (with up to a thousand TEs) and Pucciniomycetes (with several thousand TEs) (Kempken & Kück, 1998; Castanera et al., 2016; Muszewska et al., 2017).

The occurrence of ‘cut-and-paste’ transposons in many eukaryotic lineages and their similarity to the prokaryotic insertion sequences suggest that eukaryotic TEs may be older than the last common eukaryotic ancestor.

TEs shape genomes by recombination and transposition; they lead to chromosomal rearrangements; they create new gene neighbourhoods; they alter gene expression by introducing new regulatory sequences for established host genes and they play key roles in adaptation to new life styles like mutualism/symbiosis and pathogenicity by duplicating host genes, so they can take on new roles without endangering their original functions.

Pritham (2009) described eukaryotic genomes as containing:

‘…a menagerie of populations of transposable elements...’ and stated that ‘…it is evident that these elements have played an important role in genome evolution…’

TEs are thought to have been responsible for assembling the Metabolic Gene Clusters (MGC), which are common features of most fungal genomes but rarely found in other eukaryotes, though they are common in prokaryotes. MGCs are defined as:

 ‘…tightly linked sets of mostly non-homologous genes involved in a common, discrete metabolic pathway…’

They encode various functions in fungi; nutrient acquisition, synthesis and/or degradation of metabolites, etc., and are reminiscent of the developmental subroutines we discussed in Section 12.14. As well as encoding the enzymes that perform these anabolic or catabolic processes, MGCs often contain appropriate regulatory sequences, and those that code for production of toxins also include the mechanisms needed to protect their fungal resident from the toxins. This modular nature of MGCs contributes to the metabolic and ecological adaptability of fungi. MGCs enable easy pathway amplification by gene duplication, and the duplication event can also be engineered by the TEs that assembled the cluster.

Indeed, as well as assembly, TEs are capable of transposing MGCs, either to new sites in the same genome, or perhaps to other nuclei in the same heterokaryons, or to other organisms entirely. This last possibility is called horizontal gene transfer (discussed in Section 17.15 in relation to the genes coding for enzymes involved in penicillin biosynthesis). There is evidence for many horizontal gene transfer events in fungi; events that have greatly enhanced the basic lifestyle of the fungi concerned (Richards et al., 2011; Slot et al., 2017; Steenkamp et al., 2018). 

Updated July, 2018