James A. Shapiro- Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, IL, USA
Mobile DNA in the genome is subject to RNA-targeted epigenetic control. This control regulates the activity of transposons, retrotransposons and genomic proviruses. Many different life history experiences alter the activities of mobile DNA and the expression of genetic loci regulated by nearby insertions. The same experiences induce alterations in epigenetic formatting and lead to trans-generational modifications of genome expression and stability. These observations lead to the hypothesis that epigenetic formatting directed by non-coding RNA provides a molecular interface between life history events and genome alteration.
Introduction
Understanding the functional organization of the genome and its evolutionary history are key goals of modern molecular biology. The task has become more interesting and complex as we learn more the details of cell processes involving the genome. Recent applications of high resolution technologies to genome expression in animals reveal a dynamic four-dimensional interactive control architecture incompatible with prior notions that genomes contain discrete functional segments of DNA (“genes”) (Mercer and Mattick, 2013). This review will focus on the role of epigenetic regulation of viruses and mobile genetic elements as a key interface between the activities of these agents of evolutionary change and inputs from cell and organism life histories. The hypothesis developed as a result of the review is that disruption of epigenetic silencing constitutes a major target for life history activation of cellular functions for genome change. This likely occurs after genome replication, possibly by changes in small non-coding (snc) RNAs, typically on the order of 20–50 nucleotides long.
Mobile DNA is a Major and Functionally Significant Component of Genomes
One of the major surprises to come from the initial sequencing of the human genome was the high abundance of dispersed mobile repeat elements (Consortium, 2001). Today, we estimate that at least two-thirds of our genomes is composed of mobile DNA (De Koning et al., 2011). The human genome is not exceptional in its high content of mobile DNA (http://shapiro.bsd.uchicago.edu/TableII.1.shtml).
We increasingly recognize that viruses contribute to cell genomes (Kokosar and Kordis, 2013). They provide sequences for non-coding ncRNAs (Frias-Lasserre, 2012), sites for transcriptional control (Peaston et al., 2004; Dunn et al., 2005; Maksakova et al., 2006; Conley et al., 2008), and elements important in epigenetic regulation (Brunmeir et al., 2010; Conley and Jordan, 2012). Similar transcriptional and epigenetic regulatory contributions are made by mobile genetic elements (http://shapiro.bsd.uchicago.edu/Table5C-1.MobileElementsFoundtobeExaptedascis-RegulatoryControlSitesinAnimals.html) (Youngson et al., 2005; Kinoshita et al., 2007; Suzuki et al., 2007; Fujimoto et al., 2008; Gehring et al., 2009; Pask et al., 2009; Nakayashiki, 2011).
Mobile DNA is a major source of novel coding information. One mechanism is the process known as “exonization,” when splice signals are utilized in newly inserted DNA segments (http://shapiro.bsd.uchicago.edu/Origin_of_New_Protein_Domains.html). New coding sequences also form by reverse transcription of processed RNAs and genome insertion of the cDNAs, sometimes producing chimeric fusions with existing exons (http://shapiro.bsd.uchicago.edu/Table 5B. Reports of retrogenes in plant and animal genomes.html) (Long, 2001; Betrán et al., 2002; Fu et al., 2010).
It is now clear that mobile genetic elements play a key role in establishing and rewiring genomic networks (http://shapiro.bsd.uchicago.edu/Table5C-1.MobileElementsFoundtobeExaptedascis-RegulatoryControlSitesinAnimals.html) (Feschotte, 2008; Lindblad-Toh et al., 2011; Lowe et al., 2011; Testori et al., 2012; Kokosar and Kordis, 2013). Moreover, mobile element proliferation is a key factor in the formation of very large genomes (http://shapiro.bsd.uchicago.edu/Genome_Size.html).
The potential functional importance of distributed mobile DNA in genomes grows rapidly as evidence accumulates for pervasive genome transcription (http://shapiro.bsd.uchicago.edu/PervasiveGenomeTranscription.html) and for the regulatory role of non-coding RNAs (ncRNAs) in genome expression, including the functional juxtaposition of distant genome regions to activate transcription (http://shapiro.bsd.uchicago.edu/NonCodingRNAinGenomeExpression.html). Mobile elements participate in this long-range genomic communication and provide the sequences of many ncRNAs (Kapusta et al., 2013).
Cells use RNA-Targeted Epigenetic Control to Inhibit the Activity of Mobile DNA
Given the high content of mobile DNA in many genomes, an important question is: what prevents all the mobility systems from destroying genome integrity? In eukaryotic cells, a major control mechanism is sncRNA-directed epigenetic formatting into silent chromatin (Law and Jacobsen, 2010; Castel and Martienssen, 2013).
Both prokaryotes and eukaryotes have systems for capturing fragments from invading DNA molecules and placing the fragments into special loci encoding sncRNAs (Dumesic and Madhani, 2014). In prokaryotes, these loci are called CRISPRs (clustered regular interspersed palindromic repeats) (http://shapiro.bsd.uchicago.edu/CRISPRs.html) (Marraffini and Sontheimer, 2010; Garrett et al., 2011; Bikard and Marraffini, 2013; Watanabe et al., 2013). The RNA transcripts from CRISPRs are processed into sncRNAs that target cleavage of homologous invading DNA and also inactivation of complementary mRNA (Djordjevic et al., 2012). The details of the RNA processing and interference activities are well-characterized, but the acquisition of DNA fragments is poorly understood. The process must be very rapid, because viral infection yields cells that survive the initial infection with appropriate fragments added to their CRISPR repertoire (Barrangou et al., 2007).
Virtually all eukaryotes investigated, with the notable exception of budding yeast, have mechanisms for sncRNA-directed chromatin silencing. They are based on members of the Argonaute family of sncRNA-processing proteins (http://shapiro.bsd.uchicago.edu/microRNA-directedchromatinsilencing.html). Plants and animals have independently evolved distinct mechanisms of processing the sncRNAs for the Argonaute family systems, but both groups use targeted epigenetic regulatory processes to defend against virus infection (Ding and Voinnet, 2007; Csorba et al., 2009) and prevent genome instability (Table 1). Like prokaryotes, Drosophila has specific genomic loci where it acquires fragments of invading DNA to encode the targeting sncRNAs (Brennecke et al., 2007, 2008; Handler et al., 2013).
Table 1. Genome immunity by sncRNA targeting of mobile DNA (see also http://shapiro.bsd.uchicago.edu/TableII.9.shtml for earlier references).
Life History Events Destabilize Genomes and Activate Mobile DNA
Anyone who has studied real-time genome changes quantitatively knows that mutation frequencies depend upon the treatment of the experimental organism prior to measurement. A wide variety of life history events influence the natural genetic engineering (NGE) functions that generate mutations, especially mobile elements (Table 2; Shapiro, 2011). In some cases, the genome instabilities are large scale and last multiple cell or organismal generations.
Table 2. Life history events that lead to genome destabilization (see also http://shapiro.bsd.uchicago.edu/TableII.8.shtml for earlier references).
Many observations demonstrate responses of the circuits controlling NGE functions to biological and abiotic inputs. It is particularly significant that many such responses occur following exceptional cell interactions with viruses or with other cells, either by infection or by hybridization (Table 2). As we might expect, the introduction of alien DNA or chromatin into a cell often has disruptive effects on genome homeostasis (Shapiro, 2014).
Epigenetic Changes in Response to Life History Events
One of the most active research areas in the second decade of the 21st century is analyzing the impact of life history events on the epigenetic layers of cell regulatory architecture (Table 3) (Chinnusamy and Zhu, 2009a; Vandegehuchte and Janssen, 2013). The observed epigenetic responses include alterations to cytosine methylation in DNA (Chinnusamy and Zhu, 2009b), histone modifications in nucleosomes, and sncRNAs (Ruiz-Ferrer and Voinnet, 2009; Ng et al., 2012) as well as transgenerational inheritance of complex novel phenotypes (Zucchi et al., 2012), frequently induced by stress (Boyko and Kovalchuk, 2010). The phenomenon of hybrid vigor, or heterosis, increasingly is viewed as an alteration in sncRNA-targeted epigenetic formatting stimulated by the encounter of two distinct genome control regimes (Groszmann et al., 2011; Miller et al., 2012; Shivaprasad et al., 2012).
Table 3. Life history events that induce epigenetic changes (see also http://shapiro.bsd.uchicago.edu/TableII.10.shtml for earlier references).
Many of the studies demonstrating induced epigenetic modifications also document accompanying genome instabilities and emphasize their evolutionary potential (Madlung and Wendel, 2013). It is noteworthy that many of the same stimuli are involved in both genomic and epigenomic responses in plants (Hegarty et al., 2013) and animals (Arkhipova and Rodriguez, 2013). The common stimuli include infection and symbiosis (Hamon and Cossart, 2008; Bierne et al., 2012; Takahashi, 2014), hybridization and changes in ploidy.
Direct Interactions between NGE Activities and Epigenetic Regulatory Functions
In addition to disruption of sncRNA-targeted inhibition, there is limited but growing evidence that NGE functions acting on DNA molecules interact directly with epigenetic control factors. There is convincing evidence of the connection between NGE and the epigenome in DNA damage repair and retroviral or retrotransposon insertions into chromosomes.
Epigenetic Involvement in DNA Proofreading and Repair
There are recent reports that a specific histone modification (H3K36me3) primes DNA mismatch repair (Schmidt and Jackson, 2013), that H3K56 acetylation affects mismatch repair (Kadyrova et al., 2013), that hypoacetylation of H3K56 by HDACs 1 and 2 facilitates recruitment of non-homologous end-joining (NHEJ) proteins (Miller et al., 2010; Munoz-Galvan et al., 2013), and that nucleosome remodeling is integral to DS break repair (Seeber et al., 2013). Longstanding observations document the involvement of a specific histone, gamma-H2AX, in DS break repair and NHEJ (Kinner et al., 2008; Altaf et al., 2009; Dickey et al., 2009b; Redon et al., 2009; Firsanov et al., 2011; Chen et al., 2013). A direct role in chromatin remodeling for DNA repair has been claimed for another H2 analog, H2A.Z (Xu et al., 2012a).
Published reports indicate that H2AX incorporation into chromatin suppresses conversion of single-strand nicks to DS breaks (Franco et al., 2006) and affects the processing of the ends of broken DNA molecules (Helmink et al., 2011). H2AX operates in phosphorylated form (Rogakou et al., 1998; Kinner et al., 2008).
Beyond the role of H2AX, chromatin dynamics play an essential role in DNA repair and genome homeostasis (Lahue and Frizzell, 2012; Shi and Oberdoerffer, 2012). Many reports claim repair roles for chromatin regulators, remodeling complexes and nucleosome exchange factors (Ryan and Owen-Hughes, 2011):
– in DNA damage tolerance (Conaway and Conaway, 2009; Falbo et al., 2009);
– after exposure to ionizing radiation (Hunt et al., 2013);
– in UV damage responses (Palomera-Sanchez and Zurita, 2011; Yu et al., 2011);
– in DS break repair by NHEJ and HR (Van Attikum and Gasser, 2005; Williams et al., 2007; Robert et al., 2011; Xu and Price, 2011; Price and D'andrea, 2013);
– in PolyADP-dependent DNA repair (Ahel et al., 2009);
– in NER as well as DS break repair (Osley et al., 2007; Czaja et al., 2012; Yu et al., 2013a).
Nucleosome disassembly is probably necessary for certain repair processes (Linger and Tyler, 2007; Amouroux et al., 2010; Gospodinov and Herceg, 2013), and histone modifications affect damage-induced checkpoint signaling (Chen and Tyler, 2008). Once repair is complete, nucleosome modifications are reversed, and H2AX~P is eliminated from chromatin (Svetlova et al., 2010). So-called “bystander” cells, which are not subjected to DNA damage but are in the same culture as irradiated cells, also display H2AX phosphorylation (Sokolov et al., 2007; Dickey et al., 2009a, 2011).
A key feature of genome repair is that H2AX-marked damaged DNA mobilizes to subnuclear “repair centers” where homologous recombination and NHEJ proteins also localize (Lisby and Rothstein, 2005; Plate et al., 2008; Bekker-Jensen and Mailand, 2010). A role for chromatin in mobilization of damaged DNA has been proposed (Seeber et al., 2013), but multiple sources of evidence are lacking.
Retroviral and Retrotransposon Integrases
A more extensive case for NGE-chromatin interactions comes from analysis of retroviral and retrotransposon insertion specificities (Zhang and Mager, 2012). Each type of retrovirus displays a characteristic insertion specificity for its provirus (Lewinski et al., 2006). A number of targeting mechanisms involve epigenetic formatting molecules.
In budding yeast, Ty1 retrotransposon integrase contacts an H2A/H2B interface upstream of RNA polymerase III initiation sites (Baller et al., 2012; Bridier-Nahmias and Lesage, 2012; Mularoni et al., 2012). Histone deacetylase Hos2 and Trithorax group protein Set3 stimulate this nucleosome-targeted integration (Mou et al., 2006), and chromatin remodeling factor Isw2p is also implicated (Bachman et al., 2005). In contrast, the Ty5 retrotransposon inserts in silent chromatin, targeted by binding of its integrase to the Sir4 heterochromatin nucleating factor (Xie et al., 2001; Dai et al., 2007; Brady et al., 2008; Baller et al., 2011).
HIV and other lentiviral targeted integration into actively transcribed regions of the genome is associated with transcription-associated histone modifications, including H3 acetylation, H4 acetylation, and H3 K4 methylation, but is disfavored in regions rich in transcription-inhibiting modifications, which include H3K27me3 and DNA CpG methylation (Wang et al., 2007). The specificity results from integrase tethering by the LEDGF/p75 chromatin-binding growth factor (Vanegas et al., 2005; Llano et al., 2006; Ciuffi, 2008; Meehan and Poeschla, 2010; Zheng et al., 2010; Christ and Debyser, 2013). Replacing the LEDGF/p75 domain that interacts with expressed chromatin by the CBX1 domain, which binds histones H3K9me2 or H3K9me3 found in pericentric heterochromatin, targets HIV insertions to silent chromatin regions (Gijsbers et al., 2010).
Murine leukemia virus (MuLV) insertion targeting to initiation sites upstream of actively transcribed regions involves integrase interactions with bromodomain proteins BRD2, BRD3, and BRD4 (De Rijck et al., 2013; Gupta et al., 2013; Sharma et al., 2013a). Interestingly, chromatin recognition bromodomain protein BRD4 antagonizes HIV provirus reactivation (Zhu et al., 2012).
Certain retrotransposons are specifically targeted to centromeres (Wolfgruber et al., 2009; Birchler and Presting, 2012; Tsukahara et al., 2012; Sharma et al., 2013b), which have a special chromatin configuration characterized by centromeric versions of H3 (Henikoff and Dalal, 2005; Vos et al., 2006; Partridge, 2008; Zhang et al., 2008a). Centromeric retrotransposons in rice are highly associated with H3K9me2, a hallmark for heterochromatin (Neumann et al., 2007). Some centromeric retrotransposons encode integrase proteins with histone-binding chromodomains at their carboxy-termini (Neumann et al., 2011). Chromodomains recognize lysine methylation (Blus et al., 2011; Yap and Zhou, 2011; Eissenberg, 2012).
It is probably not coincidental that the most widely distributed group of retrotransposons among all eukaryotic clades are the “chromoviruses,” which are so named because they have chromodomains in their integrase proteins (Gorinsek et al., 2004; Kordis, 2005; Novikov et al., 2012; Weber et al., 2013). A chromodomain has been reported to target fungal chromovirus MAGGY insertions to heterochromatin marked by H3K9me2/me3 (Gao et al., 2008). An integrase chromodomain also participates in activator protein-targeted insertion of fission yeast retrotransposon Tf1 upstream of RNA polymerase II transcription start sites (Hizi and Levin, 2005; Chatterjee et al., 2009).
DNA Transposons
In contrast with many retrotransposons that interact with nucleosomes, the DNA transposon Hermes inserts preferentially in budding yeast into nucleosome-free regions of the genome (Gangadharan et al., 2010). The widely used P element DNA transposons in Drosophila show targeting (called “P element homing”) by incorporating binding sites for various regulatory factors, including chromatin insulators (Bender and Hudson, 2000; Fujioka et al., 2009) and Polycomb group response elements (Kassis, 2002; Cheng et al., 2012).
Epigenetic Reformatting After DNA Replication and ncRNAs as Potential Agents for Transmitting Experience to the Genome
While the evidence is increasingly abundant for effects of different life history events on epigenetic regulation in general, and on genome homeostasis in particular, it is far from clear how those effects occur (Lim and Brunet, 2013). We know very little about the connections between cell sensors and epigenetic (re)formatting complexes (Erdel et al., 2011; Narlikar et al., 2013). Deciphering those connections is currently an important research goal.
DNA replication provides a key decision point for maintaining or changing chromatin configurations (Poot et al., 2005; Liu and Gong, 2011; Mermoud et al., 2011). The replication apparatus must disassemble chromatin for polymerization and then reassemble chromatin once replication is complete. Replication takes place only in dividing cells, and transgenerational inheritance of epigenetic states must involve the proliferating cells that give rise to gametes. Transfer of outside information from somatic tissues to the germline has been reported in mammals (Sharma, 2013; Skinner et al., 2013). And epigenetic windows of susceptibility to environmental insults have been suggested during sperm development (Soubry et al., 2014). Since there is no segregated germ line in plants and eukaryotic microbes, the same cells that experience environmental inputs can also be the progenitors of gametes.
A number of different factors have been found or hypothesized to participate in post-replication chromatin restoration: histone chaperones (Budhavarapu et al., 2013), RNA editing and sncRNAs (Savva et al., 2013), chromatin remodeler SMARCAD1 (Mermoud et al., 2011), chromatin assembly factor 1 (Huang and Jiao, 2012), histone chaperon FACT (Winkler and Luger, 2011) and Swi/Snf complexes (Neves-Costa and Varga-Weisz, 2006; Ryan and Owen-Hughes, 2011; Zhu et al., 2013), and ISW1 complexes (Erdel and Rippe, 2011).
One frequently overlooked feature of post-replication reestablishment of epigenetic formatting is where in the nucleus it might occur. Replication takes place in specialized “replication factories” (Vago et al., 2009; Guillou et al., 2010). Does chromatin reestablishment occur in the same location or does it involve migration of newly replicated DNA segments to distinct subnuclear “chromatin factories,” like the ones that exist in the nucleolus for heterochromatin formation on rRNA-encoding DNA (Guetg and Santoro, 2012)? If so, such post-replication relocalization would be guided by the nucleoskeleton and lncRNAs (Mercer and Mattick, 2013; Mercer et al., 2013) and might present an attractive target for stress response and sensory input signaling (Weiner et al., 2012).
It is notable that changes to ncRNAs are frequently cited with regard to the impact of life history events on the genome (Sunkar et al., 2007; Khraiwesh et al., 2012; Lelandais-Briere et al., 2012; Nakaminami et al., 2012; Amaral et al., 2013). In the plant literature, there is documentation of numerous ncRNA changes in response to particular biotic and abiotic stress regimes (Table 4).
Table 4. Changes in non-coding RNAs in response to life history events.
A number of observations about resistance to biotic and abiotic stresses are consistent with a key role for ncRNA changes in life history responses. Several viruses encode siRNA suppressors to overcome host defenses (Jiang et al., 2012; Omarov and Scholthof, 2012; Guo and Lu, 2013). Transgenic constructs encoding constitutive miRNA expression can lead to salt and drought tolerance in creeping bentgrass (Zhou et al., 2013), to immunity against blast fungus in rice (Li et al., 2014), and in Arabidopsis to greater salt and alkalinity sensitivity (Gao et al., 2011). Acquired aphid resistance in Arabidopsis involves sncRNA changes (Kettles et al., 2013), and most acquired stress resistances in plants display transgenerational epigenetic inheritance (Holeski et al., 2012; Luna and Ton, 2012; Slaughter et al., 2012).
Speculative Conclusions about an Epigenetic Interface between Experience and Genome Change
Mobile DNA and other NGE functions are the key agents for adaptively significant changes in genome organization and DNA sequences. The data reviewed and tabulated above establish the importance of RNA-directed chromatin formatting in the regulation and operation of mobile elements, viruses and DNA repair functions. In addition, there is a remarkable correlation between the life history events that activate NGE functions to destabilize genomes and those that lead to alteration of chromatin states and DNA methylation patterns.
The preceding observations lead to the plausible hypothesis that epigenetic regulation serves as a key interface between organismal life history and the agents that restructure genomic DNA. This hypothesis is supported by the limited number of cases where empirical observations have established direct molecular connections between NGE functions and components of the epigenetic control system: histones, nucleosomes, and chromatin reformatting complexes.
If, as I expect, further research bolsters the epigenome-NGE correlations and connections documented above, then we need to ask: what components(s) of the epigenetic control apparatus communicate information about experience to NGE operators? We do not know the answer to this fundamental question. However, the data reported in Table 4 indicate that ncRNAs are good candidates for key intermediates in the experience-genome signal transduction process. If this is so, then ncRNAs are logical molecular targets for modulating genome change toward potentially adaptive outcomes. Let us hope that research aimed at examining this proposal deepens our understanding of how life history impacts both epigenetic and genome change operations (Tables 2–4), whether or not my speculation ultimately proves to be correct.
Conflict of Interest Statement
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Acknowledgments
The author is grateful to the editors for the invitation to contribute to this special issue and for the opportunity to comment on the relationship between life history and genome change.
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Keywords: mutation, evolution, natural genetic engineering, mobile DNA, viruses, mobile genetic elements, non-coding RNA
Citation: Shapiro JA (2014) Epigenetic control of mobile DNA as an interface between experience and genome change. Front. Genet. 5:87. doi: 10.3389/fgene.2014.00087
Received: 27 February 2014; Accepted: 01 April 2014;
Published online: 25 April 2014.
Edited by:
Ilaria Negri, University of Turin, ItalyReviewed by:
Jennifer Cropley, Victor Chang Cardiac Research Insitute, AustraliaMauro Mandrioli, University of Modena and Reggio Emilia, Italy
Copyright © 2014 Shapiro. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: James A. Shapiro, Department of Biochemistry and Molecular Biology, University of Chicago, GCIS W123B, 979 E. 57th Street, Chicago, IL 60637, USA e-mail: jsha@uchicago.edu