Epigenetic regulation of transposable elements in the plant kingdom

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Transposable elements (transposons, TEs, 'jumping genes') are short strands of repetitive DNA that can self-replicate and translocate within the eukaryotic genome, and are generally perceived as parasitic in nature. Their transcription can lead to the production of dsRNAs (double-stranded RNAs), which resemble retroviruses transcripts. While most host cellular RNA has a singular, unpaired sense strand, dsRNA possesses sense and anti-sense transcripts paired together, and this difference in structure allows an host organism to detect dsRNA production, and thereby the presence of transposons. Plants lack distinct divisions between somatic cells and reproductive cells, and also have, generally, larger genomes than animals, making them an intriguing case-study kingdom to be used in attempting to better understand the epigenetics function of transposable elements. [1]

Contents

Classes of Transposons

Transposons vary in their structure and manner of proliferation, both of which help to define their classification. Each class contains autonomous elements, a sub-variety distinguished by the ability to self-proliferate, and also non-autonomous elements, which lack that ability.

Class I

Also known as retrotransposons, these employ a strategy of self-copying via RNA transcriptase and subsequently inserting themselves into a new site within the host genome. The presence or absence of transcriptase (the enzyme which allows for self-copying) within the coding of the transposon defines class I elements as autonomous or non-autonomous. [2] Class I transposons can take the form of:

Curiously, retrotransposons have been discovered to be the predominant form of transpositional element in plants with large genomes, such as maize and wheat, potentially indicating rapid success of this class of transposon in the creation of hybrids, such as wheat, peppermint and, in the distant past, maize. Plant hybridization often creates polyploids, with double, triple, quadruple or more the number of chromosomes present in the parent generation. Polyploid hybrids seem to be particularly susceptible to genetic intrusion by retrotransposons, as supported by a study in sunflower hybridization, which showed that the hybridized flowers possessed genomes that were about 50% larger than that of their parents, with the majority of this increase linked to the amplification of a single retrotransposon class [3]

Class II

Also known as DNA transposons, these employ a strategy by which the transposon is excised from its position via transposase, and re-integrated elsewhere in the genome. [2] These can be identified by the following:

Those DNA transposons lacking the coding necessary to synthesize transposase function non-autonomously, likely piggy-backing off of the machinery generated by neighboring transposons of the same class. An example of this would be MITEs, miniature inverted repeat transposable elements, which, while having both TIRs and TSDs, cannot produce transposase. These are particularly prevalent in plants, and are thought to be derived from deletions in the more autonomous DNA transposons. Similarly, these types of transposons can become non-autonomous by capturing or replicating pieces of host DNA. [3]

Helitrons

Another variety of transposons, discovered in 2001, which can also potentially capture host DNA. Helitrons are thought to replicate via a "rolling circle", in which transposase links the helitron to two distinct regions of the genome at once, using a helicase, ligase, and nuclease in the process to unravel the strands involved, replicate the helitron, and subsequently ligate the replicated material into the new site. During this process, it is thought that the helitrons often encode for the surrounding DNA and integrate this into their own material. Non-autuonomous helitrons may lack a transposase, a helicase, a ligase, or a nuclease. All are thought to be necessary for this complex process of transposition. [3]

Silencing of Transposons

Due to their invasive nature, and their potentially disruptive production of ncRNAs, most transposons are dangerous to plants and metazoans alike. Given the lack of distinction between germ-line and somatic cells in the plant kingdom, this is doubly so, since alterations to the genetic and epigenetic code will be more easily inherited. [4] [3] While transposable elements may affect any number of different cell-types in an animal, be a skin cell, a liver cell, a brain cell, these changes are not heritable, due to the fact that an animal inherits only a parents gametic genetic code. In plants, however, there is no such distinction; a flower develops from a meristem, which is a form of somatic cell, and which will pass down to the flower, and thus to the offspring, any genetic or epigenetic alteration. Since each meristem will have developed differently, each different flower from each meristem of the same plant will potentially possess different modifications. In contrast to animals, however, plants do not undergo chromatin remodeling between generations, making the maintenance and inheritance of silencing an entirely different process. [4] [5] [3] There are distinct and identifiable mechanisms on the maintenance of transposon inactivation in plants but, unfortunately, there is significantly less information on initiation of said inactivation. [3]

Recognition

Though the effects of transposition can sometimes manifest phenotypically, and indeed, this effect led to their discovery, transposons can be difficult for the cellular machinery to detect. Many TEs contain stretches of genuine coding DNA, copied from the host, and there is no distinct structure, code, or identifying characteristic of any kind that would allow a cell to recognize the full range of transposable elements with accuracy. Even besides coding for functional proteins or RNAs, some transposons, like class II elements, contain code copied from the nearby strand, allowing them to blend in. Given that the preceding is true, it must be that transposons are recognized more by their effect than their structure. Thus, cell machinery, as detailed in the next section, exists that is capable of detecting transcripts that are atypical of host genomes, such as:

and, more specifically:

Methods

Silencing of transposon transcripts can vary in completeness of silencing as well as in duration of alteration. Plants employ a number of methods, which range from elimination of transcripts to complete epigenetic silencing. In general, these can be sorted into two 'strategies':

In general, initiation of transposon silencing has yet to be fully explained. For example, there have been recorded incidences[ spelling? ] of spontaneous silencing in maize, which carries a high number of transposons (~85% of the genome), though the mechanism by which this occurs is unknown. [3] While it is known that heritable methylation occurs, and must occur with frequency, and must be initiated, triggered by some distinct factor, the only known example of this is in the case of Mu killer (Muk), a gene in maize that silences MuDR, a class II autonomous transposable element. Muk encodes a natural inverted derivative of the transposase coding sequence in MuDR, which, when transcribed, forms a dsRNA that is subsequently cut into siRNA, which renders MUDR incapable of 'cutting and pasting' itself by way of RNAi interference of the transposase. Muk also engages RNAi-Directed Methylation to create a stable and heritable suppression. [2] [6]

Mutualistic/Parasitic Interactions

Though transposable elements were discovered due in large part to their deleterious effects, epigenetic research has shown that they may be, in some cases, beneficial to the host organism. [3] (1,5) This research indicates that the distinction between those two aspects, mutualist and parasite, may be harder to accurately describe than was once thought. [3]

Mutualism

The primary mutualistic interaction between transposon and host organism is in the formation of epialleles. True to the name, an epiallele is a kind of epigenetic mutant of a certain allelic type that produces distinct morphological differences from the wild type. [3] The predominant research into this subject has been conducted on Arabidopsis thaliana, which has the dual disadvantages of being both TE-poor and an overly genetically stable organism. [4] [5] [3] The manner of formation of epialleles is somewhat unclear, but it is thought to be due to the fact that some transposable elements, in stealing pieces of genetic code from their host organism, blend in so well as to confuse the host cellular machinery into thinking that its own genes are the transposons, which leads to epigenetic silencing of certain alleles, forming an epiallele. Some examples of this are:

There is also evidence to suggest that transposons play a more general role than was previously thought in the formation of miRNAs as well as in the silencing of centromeres. [7] [2]

Parasitism

Though the majority of information on transposons is in relation to their parasitic effect, it is sometimes unclear as to how exactly they hurt the host organism. To clarify, there are several ways in which a negative effect can be produced by transposable elements. [3] [4] [5] [2] [6]

Any one of these can have an extreme or minimal effect, depending on what systems the mutation affects. For example, if a transposon were to interrupt the coding for the enzyme which allows for seeds to digest the nourishing endosperm, then the seed would fail to propagate at all, meaning that the mutation was, in essence, fatal. As a counter example, a transposon could be inserted into a non-coding region (which is likely the remnant of a now inactive transposon) and have no effect at all.

Future Research

Very little is known about the initiation of epigenetic silencing of transposable elements, and aside from the rare exception to this rule, as in the gene Muk, present as an initiator of regulatory epigenetic modification in maize, there are many other unclear aspects of how transposons are regulated in plant genomes. Might they be a first step in evolution that we never knew about? [1] Might they be, simply, a kink in the chain of genetic coding, one that will eventually be worked out? Again, given the lack of information it is hard to say. Future research into this field will see the changing of our conceptions of transposons and their role in eukaryote development, one way or another.

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 is 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. Transposition often results in duplication of the same genetic material. In the human genome, L1 and Alu elements are two examples. Barbara McClintock's discovery of them earned her a Nobel Prize in 1983. Its importance in personalized medicine is becoming increasingly relevant, as well as gaining more attention in data analytics given the difficulty of analysis in very high dimensional spaces.

<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 the 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.

<span class="mw-page-title-main">DNA methylation</span> Biological process

DNA methylation is a biological process by which methyl groups are added to the DNA molecule. Methylation can change the activity of a DNA segment without changing the sequence. When located in a gene promoter, DNA methylation typically acts to repress gene transcription. In mammals, DNA methylation is essential for normal development and is associated with a number of key processes including genomic imprinting, X-chromosome inactivation, repression of transposable elements, aging, and carcinogenesis.

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.

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 is 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.

Piwi-interacting RNA (piRNA) is the largest class of small non-coding RNA molecules expressed in animal cells. piRNAs form RNA-protein complexes through interactions with piwi-subfamily Argonaute proteins. These piRNA complexes are mostly involved in the epigenetic and post-transcriptional silencing of transposable elements and other spurious or repeat-derived transcripts, but can also be involved in the regulation of other genetic elements in germ line cells.

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.

Transposon mutagenesis, or transposition mutagenesis, is a biological process that allows genes to be transferred to a host organism's chromosome, interrupting or modifying the function of an extant gene on the chromosome and causing mutation. Transposon mutagenesis is much more effective than chemical mutagenesis, with a higher mutation frequency and a lower chance of killing the organism. Other advantages include being able to induce single hit mutations, being able to incorporate selectable markers in strain construction, and being able to recover genes after mutagenesis. Disadvantages include the low frequency of transposition in living systems, and the inaccuracy of most transposition systems.

<span class="mw-page-title-main">Knockout rat</span> Type of genetically engineered rat

A knockout rat is a genetically engineered rat with a single gene turned off through a targeted mutation used for academic and pharmaceutical research. Knockout rats can mimic human diseases and are important tools for studying gene function and for drug discovery and development. The production of knockout rats was not economically or technically feasible until 2008.

RNA polymerase IV is an enzyme that synthesizes small interfering RNA (siRNA) in plants, which silence gene expression. RNAP IV belongs to a family of enzymes that catalyze the process of transcription known as RNA Polymerases, which synthesize RNA from DNA templates. Discovered via phylogenetic studies of land plants, genes of RNAP IV are thought to have resulted from multistep evolution processes that occurred in RNA Polymerase II phylogenies. Such an evolutionary pathway is supported by the fact that RNAP IV is composed of 12 protein subunits that are either similar or identical to RNA polymerase II, and is specific to plant genomes. Via its synthesis of siRNA, RNAP IV is involved in regulation of heterochromatin formation in a process known as RNA directed DNA Methylation (RdDM).

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.

Transposons are semi-parasitic DNA sequences which can replicate and spread through the host's genome. They can be harnessed as a genetic tool for analysis of gene and protein function. The use of transposons is well-developed in Drosophila and in Thale cress and bacteria such as Escherichia coli.

Transposon silencing is a form of transcriptional gene silencing targeting transposons. Transcriptional gene silencing is a product of histone modifications that prevent the transcription of a particular area of DNA. Transcriptional silencing of transposons is crucial to the maintenance of a genome. The “jumping” of transposons generates genomic instability and can cause extremely deleterious mutations. Transposable element insertions have been linked to many diseases including hemophilia, severe combined immunodeficiency, and predisposition to cancer. The silencing of transposons is therefore extremely critical in the germline in order to stop transposon mutations from developing and being passed on to the next generation. Additionally, these epigenetic defenses against transposons can be heritable. Studies in Drosophila, Arabidopsis thaliana, and mice all indicate that small interfering RNAs are responsible for transposon silencing. In animals, these siRNAS and piRNAs are most active in the gonads.

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.

Robert Anthony Martienssen is a British plant biologist, Howard Hughes Medical Institute–Gordon and Betty Moore Foundation investigator, and professor at Cold Spring Harbor Laboratory, US.

<span class="mw-page-title-main">Retrotransposon silencing</span>

Transposable elements are pieces of genetic material that are capable of splicing themselves into a host genome and then self propagating throughout the genome, much like a virus. Retrotransposons are a subset of transposable elements that use an RNA intermediate and reverse transcribe themselves into the genome. Retrotransposon proliferation may lead to insertional mutagenesis, disrupt the process of DNA repair, or cause errors during chromosomal crossover, and so it is advantageous for an organism to possess the means to suppress or "silence" retrotransposon activity.

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. It is important to note that DNA transposons do not randomly insert themselves into the genome, but rather show preference for specific sites.

<span class="mw-page-title-main">RNA-directed DNA methylation</span> RNA-based gene silencing process

RNA-directed DNA methylation (RdDM) is a biological process in which non-coding RNA molecules direct the addition of DNA methylation to specific DNA sequences. The RdDM pathway is unique to plants, although other mechanisms of RNA-directed chromatin modification have also been described in fungi and animals. To date, the RdDM pathway is best characterized within angiosperms, and particularly within the model plant Arabidopsis thaliana. However, conserved RdDM pathway components and associated small RNAs (sRNAs) have also been found in other groups of plants, such as gymnosperms and ferns. The RdDM pathway closely resembles other sRNA pathways, particularly the highly conserved RNAi pathway found in fungi, plants, and animals. Both the RdDM and RNAi pathways produce sRNAs and involve conserved Argonaute, Dicer and RNA-dependent RNA polymerase proteins.

References

  1. ↑ Jiang, Ning, Zhirong Bao, Xiaoyu Zhang, et al. "Pack-MULE transposable elements mediate gene evolution in plants." Nature. 431. (2004). Web. 20 Mar. 2014
  2. 1 2 3 4 5 Garcia-Perez, Jose L., and Martin Munoz-Lopez. "DNA Transposons: Nature And Applications In Genomics." Current Genomics: 115-128
  3. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 Lisch, Damon. "Epigenetic Regulation of Transposable Elements in Plants." Plant Biology. 60 (2009). Web. 21 Mar. 2014
  4. 1 2 3 4 5 6 Bucher, Etienne, Jon Reinders, and Marie Mirouze. "Epigenetic control of transposon transcription and mobility in Arabidopsis." Plant Biology. 15. (2012). Web. 20 Mar. 2014
  5. 1 2 3 4 Zilberman, Daniel, Terri D. Bryson, Steven Henikoff, et al. " Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis." Genome Biology. (2005). Web. 8 Mar. 2014
  6. 1 2 Slotkin, R. Keith, Michael Freeling, and Damon Lisch. "Mu killer Causes the Heritable Inactivation of the Mutator Family of Transposable Elements in Zea mays." Genetics Society of America
  7. ↑ Lisch, Damon. "Epigenetic Regulation of Transposable Elements in Plants." Plant Biology. 60 (2009). Web. 21 Mar. 2014.Lisch, Damon. "Epigenetic Regulation of Transposable Elements in Plants." Plant Biology. 60 (2009). Web. 21 Mar. 2014
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