Starship (genetics)

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Starships are a type of eukaryotic class 2 transposable element (TE). They are mobilized by a site-specific recombinase termed the "captain". They are strictly found within fungi of the subphylum Pezizomycotina, where they appear to be widespread. They are characterized by a number of features that separate them from typical TEs. Given Starship elements are generally found in only a single copy in a genome, whereas other TEs are almost universally multicopy. In addition to the captain, Starships are observe to carry a large diversity of additional genes termed cargo. These genes largely appear to be acquired from fungal genomes, but the mechanism of capture is unknown. Cargo genes can have important impacts of host phenotypes, including plant pathogenicity, heavy metal resistance, and cheese production. [1] Due to the inclusion of additional genes, Starships are considerably larger than typical DNA transposons, with a current distribution between 25 kb and 700 kb. [2]

Contents

History

Starships were discovered and named in a 2022 publication, however many other genomic regions were retroactively determined to be Starships. These include: the region containing the ToxA plant effector gene from Pyrenophora tritici-repentis , Wallaby and CheesyTer from species of Penicillium used in cheese production, and segmental duplications in the human fungal pathogen Aspergillus fumigatus . [1]

Structure

Starships lack the large structural features that comprise other TEs, such as terminal inverted repeats (TIRs) and do not create target site duplications (TSDs) when they transpose, as the recombinase activity does not generate sticky ends. Instead, their boundaries are defined by short direct repeats (DRs). Some Starships possess short asymmetric TIRs, which are often imperfect, but it is unclear if these are an absolute requirement for delineating the element's boundaries. Being site-specific, Starships insert themselves at specific target sites in the genome. [2] These sites may be highly specific, such as targeting the 5S ribosomal RNA gene, or AT-rich sequence.

Genome-wide identification

The low copy number of Starships makes their identification and annotation difficult as typical software for repeat annotation relies on identifying repetitive sequences. To remedy this, a pipeline called starfish has been developed. It operates by first generating gene models for all putative captain sequences within a genome. Then, large insertions that contain captain genes are identified based on alignments to closely related genomes. The software attempts to look for DRs and TIRs to define element boundaries. Lastly, flanking genes are identified through orthogroup assignment to locate the genomic position of each Starship. Large-scale genome mining using the software has identified hundreds of Starships across fungal genomes.

Horizontal transfer

Horizontal gene transfer (HGT) refers to the movement of genetic information between individuals, and contrasts to the vertical inheritance that occurs when genes are passed from parent to offspring. A striking feature of Starships is that given elements are repeatedly observed in individuals of different taxa. For example, Hephaestus is nearly identical across over 80 kb of sequences between Paecilomyces variotii and Penicillium chermesium. The use of whole genome comparisons indicates that the reason for the high similarity is that Starships are frequently transferred horizontally between individuals. As these Starships often harbour fungal genes with impacts on host phenotype, these transfers are likely beneficial to the host.

Evolutionary implication

The Starships represent a unique mechanism among eukaryotes through which fungi can adapt. The transfer of genes with adaptive functions via mobile genetic elements is well established in prokaryotes, where it is important for phenomena such as antimicrobial resistance. The discovery of a parallel system in fungi implies that HGT should be regarded as a recurrent mode of evolution in these fungi, not as a rare chance occurrence. [2]

Related Research Articles

<span class="mw-page-title-main">Genome</span> All genetic material of an organism

In the fields of molecular biology and genetics, a genome is all the genetic information of an organism. It consists of nucleotide sequences of DNA. The nuclear genome includes protein-coding genes and non-coding genes, other functional regions of the genome such as regulatory sequences, and often a substantial fraction of junk DNA with no evident function. Almost all eukaryotes have mitochondria and a small mitochondrial genome. Algae and plants also contain chloroplasts with a chloroplast genome.

<span class="mw-page-title-main">Transposable element</span> Semiparasitic DNA sequence

A transposable element (TE), also transposon, or jumping gene, is a type of mobile genetic element, a nucleic acid sequence in DNA that can change its position within a genome, sometimes creating or reversing mutations and altering the cell's genetic identity and genome size.

<span class="mw-page-title-main">Horizontal gene transfer</span> Transfer of genes from unrelated organisms

Horizontal gene transfer (HGT) or lateral gene transfer (LGT) is the movement of genetic material between organisms other than by the ("vertical") transmission of DNA from parent to offspring (reproduction). HGT is an important factor in the evolution of many organisms. HGT is influencing scientific understanding of higher-order evolution while more significantly shifting perspectives on bacterial evolution.

<span class="mw-page-title-main">Retrotransposon</span> Type of genetic component

Retrotransposons are mobile elements which move in the host genome by converting their transcribed RNA into DNA through reverse transcription. Thus, they differ from Class II transposable elements, or DNA transposons, in utilizing an RNA intermediate for the transposition and leaving the transposition donor site unchanged.

P elements are transposable elements that were discovered in Drosophila as the causative agents of genetic traits called hybrid dysgenesis. The transposon is responsible for the P trait of the P element and it is found only in wild flies. They are also found in many other eukaryotes.

In biology, a gene cassette is a type of mobile genetic element that contains a gene and a recombination site. Each cassette usually contains a single gene and tends to be very small; on the order of 500–1,000 base pairs. They may exist incorporated into an integron or freely as circular DNA. Gene cassettes can move around within an organism's genome or be transferred to another organism in the environment via horizontal gene transfer. These cassettes often carry antibiotic resistance genes. An example would be the kanMX cassette which confers kanamycin resistance upon bacteria.

Exon shuffling is a molecular mechanism for the formation of new genes. It is a process through which two or more exons from different genes can be brought together ectopically, or the same exon can be duplicated, to create a new exon-intron structure. There are different mechanisms through which exon shuffling occurs: transposon mediated exon shuffling, crossover during sexual recombination of parental genomes and illegitimate recombination.

<span class="mw-page-title-main">Mobile genetic elements</span> DNA sequence whose position in the genome is variable

Mobile genetic elements (MGEs), sometimes called selfish genetic elements, are a type of genetic material that can move around within a genome, or that can be transferred from one species or replicon to another. MGEs are found in all organisms. In humans, approximately 50% of the genome are thought to be MGEs. MGEs play a distinct role in evolution. Gene duplication events can also happen through the mechanism of MGEs. MGEs can also cause mutations in protein coding regions, which alters the protein functions. These mechanisms can also rearrange genes in the host genome generating variation. These mechanism can increase fitness by gaining new or additional functions. An example of MGEs in evolutionary context are that virulence factors and antibiotic resistance genes of MGEs can be transported to share genetic code with neighboring bacteria. However, MGEs can also decrease fitness by introducing disease-causing alleles or mutations. The set of MGEs in an organism is called a mobilome, which is composed of a large number of plasmids, transposons and viruses.

In the fields of bioinformatics and computational biology, Genome survey sequences (GSS) are nucleotide sequences similar to expressed sequence tags (ESTs) that the only difference is that most of them are genomic in origin, rather than mRNA.

In biology, phase variation is a method for dealing with rapidly varying environments without requiring random mutation. It involves the variation of protein expression, frequently in an on-off fashion, within different parts of a bacterial population. As such the phenotype can switch at frequencies that are much higher than classical mutation rates. Phase variation contributes to virulence by generating heterogeneity. Although it has been most commonly studied in the context of immune evasion, it is observed in many other areas as well and is employed by various types of bacteria, including Salmonella species.

<span class="mw-page-title-main">LTR retrotransposon</span> Class I transposable element

LTR retrotransposons are class I transposable elements (TEs) characterized by the presence of long terminal repeats (LTRs) directly flanking an internal coding region. As retrotransposons, they mobilize through reverse transcription of their mRNA and integration of the newly created cDNA into another genomic location. Their mechanism of retrotransposition is shared with retroviruses, with the difference that the rate of horizontal transfer in LTR-retrotransposons is much lower than the vertical transfer by passing active TE insertions to the progeny. LTR retrotransposons that form virus-like particles are classified under Ortervirales.

Helitrons are one of the three groups of eukaryotic class 2 transposable elements (TEs) so far described. They are the eukaryotic rolling-circle transposable elements which are hypothesized to transpose by a rolling circle replication mechanism via a single-stranded DNA intermediate. They were first discovered in plants and in the nematode Caenorhabditis elegans, and now they have been identified in a diverse range of species, from protists to mammals. Helitrons make up a substantial fraction of many genomes where non-autonomous elements frequently outnumber the putative autonomous partner. Helitrons seem to have a major role in the evolution of host genomes. They frequently capture diverse host genes, some of which can evolve into novel host genes or become essential for Helitron transposition.

A conserved non-coding sequence (CNS) is a DNA sequence of noncoding DNA that is evolutionarily conserved. These sequences are of interest for their potential to regulate gene production.

The Sleeping Beauty transposon system is a synthetic DNA transposon designed to introduce precisely defined DNA sequences into the chromosomes of vertebrate animals for the purposes of introducing new traits and to discover new genes and their functions. It is a Tc1/mariner-type system, with the transposase resurrected from multiple inactive fish sequences.

Miniature Inverted-repeat Transposable Elements (MITEs) are a group of non-autonomous Class II transposable elements. Being non-autonomous, MITEs cannot code for their own transposase. They exist within the genomes of animals, plants, fungi, bacteria and even viruses. MITEs are generally short elements with terminal inverted repeats and two flanking target site duplications (TSDs). Like other transposons, MITEs are inserted predominantly in gene-rich regions and this can be a reason that they affect gene expression and play important roles in accelerating eukaryotic evolution. Their high copy number in spite of small sizes has been a topic of interest.

Ac/Ds transposable controlling elements was the first transposable element system recognized in maize. The Ac Activator element is autonomous, whereas the Ds Dissociation element requires an Activator element to transpose. Ac was initially discovered as enabling a Ds element to break chromosomes. Both Ac and Ds can also insert into genes, causing mutants that may revert to normal on excision of the element. The phenotypic consequence of Ac/Ds transposable element includes mosaic colors in kernels and leaves in maize.

DNA transposons are DNA sequences, sometimes referred to "jumping genes", that can move and integrate to different locations within the genome. They are class II transposable elements (TEs) that move through a DNA intermediate, as opposed to class I TEs, retrotransposons, that move through an RNA intermediate. DNA transposons can move in the DNA of an organism via a single-or double-stranded DNA intermediate. DNA transposons have been found in both prokaryotic and eukaryotic organisms. They can make up a significant portion of an organism's genome, particularly in eukaryotes. In prokaryotes, TE's can facilitate the horizontal transfer of antibiotic resistance or other genes associated with virulence. After replicating and propagating in a host, all transposon copies become inactivated and are lost unless the transposon passes to a genome by starting a new life cycle with horizontal transfer. DNA transposons do not randomly insert themselves into the genome, but rather show preference for specific sites.

Plant–fungus horizontal gene transfer is the movement of genetic material between individuals in the plant and fungus kingdoms. Horizontal gene transfer is universal in fungi, viruses, bacteria, and other eukaryotes. Horizontal gene transfer research often focuses on prokaryotes because of the abundant sequence data from diverse lineages, and because it is assumed not to play a significant role in eukaryotes.

Metabolic gene clusters or biosynthetic gene clusters are tightly linked sets of mostly non-homologous genes participating in a common, discrete metabolic pathway. The genes are in physical vicinity to each other on the genome, and their expression is often coregulated. Metabolic gene clusters are common features of bacterial and most fungal genomes. They are less often found in other organisms. They are most widely known for producing secondary metabolites, the source or basis of most pharmaceutical compounds, natural toxins, chemical communication, and chemical warfare between organisms. Metabolic gene clusters are also involved in nutrient acquisition, toxin degradation, antimicrobial resistance, and vitamin biosynthesis. Given all these properties of metabolic gene clusters, they play a key role in shaping microbial ecosystems, including microbiome-host interactions. Thus several computational genomics tools have been developed to predict metabolic gene clusters.

hAT transposons are a superfamily of DNA transposons, or Class II transposable elements, that are common in the genomes of plants, animals, and fungi.

References

  1. 1 2 Gluck-Thaler E, Ralston T, Konkel Z, Ocampos CG, Ganeshan VD, Dorrance AE, et al. (May 2022). Larracuente A (ed.). "Giant Starship Elements Mobilize Accessory Genes in Fungal Genomes". Molecular Biology and Evolution. 39 (5). doi:10.1093/molbev/msac109. PMC   9156397 . PMID   35588244.
  2. 1 2 3 Urquhart A, Vogan AA, Gluck-Thaler E (December 2024). "Starships: a new frontier for fungal biology". Trends in Genetics. 40 (12). doi:10.1016/j.tig.2024.08.006.