recent spread of a retrotransposon in the silene latifolia - genetics

Copyright � 2009 by the Genetics Society of AmericaDOI: 10.1534/genetics.108.099267

Note

Recent Spread of a Retrotransposon in the Silene latifolia Genome,Apart From the Y Chromosome

Dmitry A. Filatov,*,1 Elaine C. Howell,† Constantinos Groutides† and Susan J. Armstrong†

*Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, United Kingdom and †School of Biosciences,University of Birmingham, Birmingham B15 2TT, United Kingdom

Manuscript received December 2, 2008Accepted for publication December 8, 2008

ABSTRACT

Transposable elements often accumulate in nonrecombining regions, such as Y chromosomes. Contraryto this trend, a new Silene retrotransposon described here, has spread recently all over the genome ofplant Silene latifolia, except its Y chromosome. This coincided with the latest steps of sex chromosomeevolution in this species.

TRANSPOSABLE elements (TEs) are ubiquitous inpro- and eukaryotic genomes. Plant genomes

appear to be particularly littered with various families ofretrotransposons, the elements that transpose via anRNA intermediate. For example, .75% of the maizegenome and large proportions of genomes of othercrops are composed of retrotransposons (Meyers et al.2001; Schulman and Kalendar 2005).

The evolutionary dynamics of TEs is dominated byperiods of active transposition (Bingham et al. 1982;Biemont et al. 1994; Petrov et al. 1995; Nuzhdin et al.1997; Naito et al. 2006; Bergman and Bensasson 2007),which may lead to dramatic expansion of copy numberof the particular element and even to a significantincrease in genome size (Neumann et al. 2006; Hawkins

et al. 2008). The periods of active transpositions arefollowed by periods of inactivity that may eventually leadto extinction of the particular transposable element.Such ‘‘boom and bust’’ cycles of TE activity may resultfrom a combination of several factors. One reasonablywell-documented factor is invasion by a new TE of aspecies that previously lacked it (Daniels et al. 1990;Kidwell 1992; Lohe et al. 1995; Clark and Kidwell

1997; Silva and Kidwell 2004; Sanchez-Gracia et al.2005; Diao et al. 2006). Over 100 horizontal transferevents of TEs of various kinds have been reported forDrosophila alone (Loreto et al. 2008). The mecha-nisms of TE horizontal transfer are not known, but atleast for long terminal repeat (LTR) retrotransposons it

can be hypothesized that horizontal transfer occurs viathe mechanisms similar to that of retroviral infections,as LTR retrotransposons are very closely related toretroviruses and are capable of forming virus-like par-ticles (Miyake et al. 1987).

We describe a relatively recent ‘‘burst’’ of transposi-tion activity of a new LTR retrotransposon in the plantSilene latifolia (Caryophyllaceae) and its close relatives.One of the most interesting features of this species is thepresence of sex chromosomes that determine whetherthe plant develops as a male with XY chromosomes ora female with XX sex chromosomes (Westergaard

1958). The sex chromosomes in Silene evolved rel-atively recently, probably �107 years ago (Filatov andCharlesworth 2002) within a small cluster of dioe-cious Silene species, (section Elisanthe), while the restof the genus is mostly nondioecious. S. latifolia sex chro-mosomes apparently evolved from a single pair ofautosomes that ceased recombining with each otheralong most of their length and began to diverge(Filatov 2005a). This process occurred in at least threesteps (Nicolas et al. 2005; Bergero et al. 2007), resem-bling ‘‘evolutionary strata’’ discovered on the humansex chromosomes (Lahn and 999). The X/Ysilent divergence in the oldest ‘‘stratum’’ on the S. latifoliasex chromosomes is only �15–24% and the youngeststratum shows only 2–4% divergence (Bergero et al.2007). Assuming the substitution rate of 1.05 3 10�8 persilent site per year (Derose-Wilson and Gaut 2007),the age of the oldest part of the S. latifolia sex chromo-somes might be �10 million years old and the youngestregion may be as young as 2 million years old. However,this estimate is rough, as substitution (and mutation)

1Corresponding author: Department of Plant Sciences, University ofOxford, South Parks Rd., Oxford OX1 3RB, United Kingdom.E-mail: [email protected]

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rates may vary between genes and between species andthe exact rate of molecular clock in S. latifolia is notknown. The S. latifolia X and Y still pair and recombinein male meiosis in a small pseudoautosomal region(PAR) (reviewed in Armstrong and Filatov 2008).

Evolution of sex chromosomes is expected to lead todegeneration of Y-linked genes due to lack of recombi-nation that slows down adaptive evolution (Rice 1987)and exacerbates the processes of genetic hitchhiking,background selection, and Muller’s ratchet that lead toaccumulation of deleterious mutations and gene loss(reviewed in Charlesworth 1991, 2008). Accumulationof TE insertions and other repetitive DNA is also a typicalfeature of Y chromosomes as in degenerate Y chrom-osomes TE insertions are less likely to damage impor-tant genes and lack of recombination prevents ectopicexchange between the TE copies (Charlesworth et al.1994; Abe et al. 2005; Steinemann and Steinemann

2005).Despite its relatively recent origin, S. latifolia

Y chromosome shows some signs of genetic degenera-tion, including drastic reduction of DNA polymorphism(Filatov et al. 2000; Ironside and Filatov 2005),accumulation of mutations at sites that are known to beimportant for the functional activity of proteins (Filatov

2005b), and gene expression changes (Marais et al.2008). Accumulation of repetitive DNA on the S. latifoliaY chromosome has also been reported (Hobza et al. 2006;Kejnovsky et al. 2006; Kazama and Matsunaga 2008).Below we describe the opposite trend—accumulation ofa transposable element all over the S. latifolia genome,

except the Y chromosome. This unusual genomic distri-bution of the transposable element provides a useful‘‘negative paint’’ for the S. latifolia Y chromosome andallows visualizing regions of the Y chromosome that havedifferent evolutionary histories.

Identification and genomic distribution of a newretrotransposon: As a by-product of a continuing effortto isolate more S. latifolia sex-linked genes, we identifieda fosmid clone that gave an unusual FISH signal. TheFISH signal was frequent and widely distributed, sug-gesting the presence of an abundant repeat in thisfosmid. However, there was considerably less hybridiza-tion to the majority of the Y chromosome. To investigatethe cause of this peculiar distribution, we subclonedfragments of the fosmid and used the subclones asprobes for FISH. We identified several subclones thatresulted in a hybridization pattern similar to the originalfosmid (Figure 1, a and b, and, supplemental Figure S1).These clones were sequenced and blast searched againstthe nr NCBI database. This revealed similarity to variousretrotransposons, with the closest match to the Viciaretrotransposon Ogre (GenBank accession AY936172).One of these clones (clone 4.2), contained an openreading frame with a strong match to Ogre reversetranscriptase, and this clone was used for furtheranalyses. Comparative phylogenetic analysis of the pro-tein sequences of the reverse transcriptases of variousretrotransposons confirmed that the newly identifiedelement clusters with Ogre retrotransposons from otherplant species (supplemental Figure S2). According tothe naming convention proposed by Capy (2005), we

Figure 1.—Fluorescence in situ hybridization(FISH) with Silene chromosomes counterstainedwith DAPI (blue). (a–d) FISH with SlOgre1, clone4.2 (green signal) on metaphase 1 spreads of (a)S. latifolia, (c) S. dioica, and (d) S. marizii. Whitearrow indicates the XY bivalent. (b) S. latifolia,with green filter only, showing the extent of hy-bridization at the PAR end of the Y chromosome(white arrowhead). (e) Mitotic metaphase of S.vulgaris probed with SlOgre1, clone 4.2, no hybrid-ization detected. (f–j) Dual probe FISH with S.latifolia chromosomes. SlOgre1, clone 4.2, (green)and SlCypY gene (red). Open (black) arrowheadindicates the PAR region and open arrow pointsto SlCypY signal on the Y chromosome. (f–h) Mi-totic metaphase. (i) Partial mitotic metaphase.( j) Partial meiotic metaphase 1. (f and g) Sequen-tial probing with images merged, some overlap ofautosomes and Y is visible. (h–j) Simultaneousprobing with clone 4.2 and SlCypY probes. (j) NoteSlCyp (red) signal on the X chromosome; due tolow X/Y divergence in this gene the SlCypY probehybridizes with the X-linked homolog of SlCypYgene. Bar, 10 mm is shown at the bottom of eachpanel. For details of in situ hybridization proce-dure see legend of supplemental Figure S1.

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named the newly identified S. latifolia retrotransposonSlOgre1.

A plausible explanation of the apparent absence ofthe SlOgre1 from the Y chromosome may be trans-position of that element in S. latifolia females only. Suchsex specificity is not uncommon among TEs. For ex-ample, the Drosophila melanogaster retrotransposon copiais preferentially transcribed and transposed in malegerminal tissues, while another D. melanogaster TE, Doc,transposes only in female germinal tissues (Filatov

et al. 1998; Pasyukova et al. 1998). In fact, TE expressionand transposition can be very specific, depending onvarious factors such as stress (Grandbastien et al. 2005)or age (Filatov et al. 1998).

To test whether there is a difference in transcriptabundance between the sexes, we conducted PCRamplification of reverse transcribed total RNA fromflower buds and leaves of S. latifolia males and females,but no amplification of the SlOgre1 sequence wasobserved in either sex. A fragment of SlssX/Y gene wassuccessfully amplified from the same reverse tran-scribed RNA samples with primers Slss11 and Slss�2(Filatov 2005b), which was used as a control for RNAand cDNA quality (data not shown). This region of theSlssX/Y gene contains a short (240-bp-long) intron ingenomic DNA, but not in the PCR product amplifiedfrom the reverse transcribed RNA samples, demonstrat-ing that the PCR product could not have been a result ofcontamination of cDNA with genomic DNA. This isconsistent with the view that SlOgre1 may not be activeany more (see below). The negative result with RT–PCRof testing for SlOgre1 expression does not necessarilymean that this element is completely inactive; it couldstill be expressed at a low level in some tissues. This hasnot been investigated further, as the activity/inactivity ofthe element is not the central question of this work anddoes not affect our conclusions.

To investigate the distribution of SlOgre1 in S. latifoliarelatives, we conducted FISH with clone 4.2 in threeother dioecious Silene species that also belong tosection Elisanthe, S. dioica, S. diclinis, and S. marizii, aswell as with nondioecious S. vulgaris. The distribution ofFISH signal in the dioecious species is very similarto that in S. latifolia: the probe paints the autosomesand the X chromosome, but leaves the majority of theY chromosome ‘‘unpainted’’ (Figure 1, c and d). Thesespecies are very closely related and are likely to haveseparated within the last 1–2 million years, since nuclearDNA divergence at silent sites does not exceed 2%(Ironside and Filatov 2005; Laporte et al. 2005; Muir

and Filatov 2007). Therefore, this result is not entirelyunexpected. On the other hand, there is no signal onS. vulgaris chromosomes (Figure 1e), suggesting thatSlOgre1 is not present in multiple copies in S. vulgaris.Alternatively, the lack of FISH signal in S. vulgaris couldbe due to divergence between the S. latifolia and S.vulgaris sequences (�15% for silent sites, see Filatov

and Charlesworth 2002), precluding effective in situhybridization. However, the low divergence between thecopies of the element present within S. latifolia (seebelow) suggests that SlOgre1 started to actively transposequite recently in S. latifolia and its relatives (or theirancestor), providing additional support to the view thatthis TE has not been widespread in the S. vulgaris genome.

The recent spread of the retrotransposon: Therelatively recent origin of S. latifolia sex chromosomesand the lack of accumulation of SlOgre1 on the majorityof the Y chromosome provide an evolutionary perspec-tive on the dynamics of the SlOgre1 retrotransposonspread. As the S. latifolia Y chromosome recombinedwith the X chromosome before cessation of recombi-nation on the Y chromosome, the Y chromosome shouldcontain approximately the same number of copies ofthe retrotransposon, unless either the copies have beenspecifically removed from the Y or the transposableelements started to actively spread after the X and Ystopped recombining. To estimate more precisely thetiming of spread of SlOgre1 in the genomes of dioeciousSilene section Elisanthe, we measured divergence be-tween the copies of SlOgre1 in four Elisanthe species. Forthis purpose we PCR amplified, cloned, and sequenceda 1.2-kb-long fragment of the SlOgre1 elements from onemale individual from each of the four closely relateddioecious Silene species: S. latifolia, S. dioica, S. marizii,and S. diclinis. An attempt to amplify the retrotransposonfrom S. vulgaris with three different pairs of primers wasunsuccessful, which is in line with lack of hybridizationof the element with S. vulgaris chromosomes.

The phylogeny of the 90 sequenced copies of SlOgre1elements from four species is shown in Figure 2 andsupplemental Figure S3. Interestingly, the sequences donot cluster by species, which supports the view that thiselement spread before divergence of these species.However, gene flow between these species may alsocreate the same effect. All crosses among S. latifolia,S. dioica, S. marizii, and S. diclinis yield viable and fertileprogeny, except S. latifolia 3 S. diclinis cross, which oftenyields only few or no viable progeny (Prentice 1978).S. marizii and S. diclinis are Iberian endemics with fairlyrestricted ranges that do not overlap (Prentice 1976,1977). Only S. latifolia is present in the ranges [but not inthe same locations (D. A. Filatov, personal observation)]of the two Iberian endemics, but hybrids between thesespecies have not been reported in the wild. S. latifoliaand S. dioica are widely distributed across Europe butinhabit somewhat different habitats: S. latifolia is com-mon in open fields and along the roads, while S. dioicaprefers more shady and wet forest habitats. The twospecies are known to form hybrids in contact zones,which are often habitats disturbed by human activity(Backer 1948). Thus, it seems likely that until very re-cently S. latifolia and S. dioica have not actively exchangedgenes. Indeed, our multigenic study of DNA polymor-phism and divergence between these two species has

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not provided any evidence for historical long-term geneflow (G. Muir, A. Harper and D. A. Filatov, unpub-lished results). Thus, lack of species clustering of theSlOgre1 copies is probably due to active transpositionprior to speciation in Silene section Elisanthe rather thandue to gene flow between these species.

The overall shape of the tree suggests that theretrotransposon has spread across the genome in arelatively short period of time and may not be active anymore—the internal branches of the tree are quite short,while the external branches are relatively long, so thetree resembles a multirayed star (Figure 2). Fu and Li’sD* statistic (Fu and Li 1993) that effectively comparesthe lengths of external and internal branches of the treeis significantly negative (D* ¼ �4.4, P , 0.02) confirm-ing that the external branches are stretched, relative tothe internal branches. If SlOgre1 elements were stillactively transposing, one would expect to see a morebalanced tree, with many relatively recent branchingpoints (Brookfield 2005; Brookfield and Johnson

2006), which is not the case.The presence of multiple in-frame stop codons and

frameshift deletions also agrees with the lack of recenttransposition activity: almost half of the sequences fromall four species (40 of 90) contained at least one stop

codon in the open reading frame (ORF). Of the re-maining 50 sequences without in-frame stop codons,8 contained frameshift deletions. Given that the se-quenced region represented only a small fraction of theelement length, it seems likely that most copies of theretrotransposon might have damaged ORFs or encodenonfunctional proteins.

To estimate the age distribution of individual SlOgre1copies we used the length of external branches forsynonymous sites as a proxy for the age of individualretrotransposon copies. The distribution of branchlength in all four species peaks at �4.5% (Figure 3) andthe distributions are not significantly different amongthe four species (Kolmogorov–Smirnov two sample tests,P . 0.14; also see supplemental Figure S4). Assuming asubstitution rate of 1.05 3 10�8 per site per year (Derose-Wilson and Gaut 2007), the transposition activity ofSlOgre1 peaked �5 million years ago. However, the truesubstitution rate of TEs in S. latifolia is not known and maybe higher than for other genomic regions as the RNAintermediate and reverse transcription step in the retro-element life cycle may result in a higher mutation rate forsuch elements, compared to the rest of the genome. Inthat case the peak of SlOgre1 transposition activity wouldbe more recent.

Figure 2.—Neighbor-joining tree of SlOgre1 se-quences from four closelyrelated dioecious Silenespecies. The branch lengthsreflect Jukes–Cantor (Jukes

and Cantor 1969) nucleo-tide distances between thesequences (all sites). For de-tails of PCR amplificationand sequencing conditionssee legend of supplementalFigure S3. All sequenceswere deposited into Gen-Bank under accession nos.FJ531702–FJ531791.


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The recent spread of SlOgre1 in Silene sectionElisanthe may have followed a horizontal transfer ofthis element from an unknown plant species. Theclosest known SlOgre1 relatives are present in legumes,but these sequences are too diverged from SlOgre1(supplemental Figure S2) to be considered as immedi-ate ancestors. Ogre elements are closely related to theretrotransposon gypsy, which is effectively a retrovirusand has an env gene, encoding a product essential forthe ability of the virus-like particles to leave the host cellsand infect other cells. Indeed, infectivity of gypsyelements has been demonstrated in Drosophila (Kim

et al. 1994).The spread of SlOgre1 and sex chromosome evolu-

tion in Silene: Different sections of the S. latifoliaY chromosomes ceased to recombine with the X atdifferent times in the past, creating evolutionary strata(Filatov 2005a; Nicolas et al. 2005; Bergero et al.2007). If SlOgre1 transpositions occur only in females,then this TE is expected to be absent only from the strataon the Y that are older than the time of the elementspread. Younger strata will have been pseudoautosomalat the time of most active transpositions of the element;hence they might contain as many copies on theY chromosome as the corresponding region on the X.To test whether the SlOgre1 is most abundant in theyoungest stratum of the S. latifolia Y chromosome, wehybridized preparations of chromosomes with two

probes, the clone 4.2 and a probe to a Y-linked geneSlCypY. The divergence between the SlCypX and SlCypYgenes is only 4% at silent sites, placing this gene into theyoungest stratum (Bergero et al. 2007). However, it isclear from Figure 1, f–j, that the SlOgre1 FISH signaldoes not spread as far as the SlCypY gene. This maysuggest that the spread of the SlOgre1 element is morerecent than the cessation of recombination betweenthe X and Y chromosomes in the most recent stratum.The weak signal of SlOgre1 hybridization with the Ychromosome (Figure 1, a–c) may be due to cross-hybridization with other repeats on the Y, or to the pres-ence of fragments or full-length copies of SlOgre1 on theY chromosome (perhaps transposed to the Y by otherTEs).

Alternatively, the position of the SlCypY gene may notbe as close to the PAR as expected on the basis of theposition of its X-linked homolog in the genetic map ofthe X chromosome (Bergero et al. 2007). The order ofS. latifolia Y-linked genes may have been changed dueto multiple rearrangements (Bergero et al. 2008). Suchrearrangements have been reported for the Y chromo-somes of other species, e.g., while the order of genes onthe human X chromosome corresponds to that ex-pected from the evolutionary strata model, the order ofthe genes on the Y chromosome have been considerablyaltered (Lahn and Page 1999; Graves 2006). Accord-ing to our FISH mapping, the SlCypY gene, is locatedclose to PAR of the Y chromosome (Figure 1, f–j)whereas deletion mapping of the Y chromosome tenta-tively placed SlCypY on the opposite arm (Bergero et al.2008). This can be explained if different accessions haverearrangements of the order of Y-linked genes, forwhich Bergero et al. (2008) have provided evidence.

Although it is not completely clear how far into thenonrecombining portion of the Y chromosome theSlOgre1 element has spread, this element will still beuseful as a negative paint for the dioecious Silenesection Elisanthe Y chromosome. For example, it mayhelp to resolve the controversy regarding the presenceof a second PAR in S. latifolia. According to an AFLP mapof S. latifolia sex chromosomes, recombination betweenX and Y occurs on both arms of the Y chromosome(Scotti and Delph 2006), suggesting the presence of asecond PAR. We could not see any evidence for a secondPAR in our accession (IL25, Kidderminster, UnitedKingdom) using clone 4.2 as a FISH probe, but it ispossible that accessions may differ in this respect. Thismay be tested by analyzing more accessions with thenegative paint for the Y chromosome reported in thisarticle. It may also be feasible to use this probe toestimate the relative size of the PAR in S. latifolia. On thebasis of our FISH results with the clone 4.2 probe wesuggest that the S. latifolia PAR is much less than 10% ofthe Y length; however, it is difficult to be more precise.Electron microscopy analysis of the PAR region mayyield more precise estimates.

Figure 3.—Age distribution of SlOgre1 insertions. Fre-quency histogram of terminal branch length for synonymoussites (Nei–Gojobori distance (Nei and Gojobori 1986) withJukes–Cantor correction (Jukes and Cantor 1969), calcu-lated in MEGA4 (Tamura et al. 2007) in four closely relateddioecious Silene species. The external branch lengths weremanually typed into Microsoft Excel and the histogram ofbranch lengths was created using the ‘‘histogram’’ option inthe data analysis pack of Excel 2007.

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We are grateful to Thomas Meagher for providing S. marizii seeds andto Deborah Charlesworth and two anonymous reviewers for helpfulcomments. The work was funded by a grant from the Biotechnology andBiological Sciences Research Council to D.A.F. and S.J.A.

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Communicating editor: D. Charlesworth

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recent spread of a retrotransposon in the silene latifolia - genetics

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