review article rna-mediated gene duplication and...

Hindawi Publishing CorporationInternational Journal of Evolutionary BiologyVolume 2013 Article ID 424726 16 pageshttpdxdoiorg1011552013424726

Review ArticleRNA-Mediated Gene Duplication and Retroposons RetrogenesLINEs SINEs and Sequence Specificity

Kazuhiko Ohshima

Graduate School of Bioscience Nagahama Institute of Bio-Science and Technology Nagahama 526-0829 Japan

Correspondence should be addressed to Kazuhiko Ohshima k ohshimanagahama-i-bioacjp

Received 14 May 2013 Accepted 1 July 2013

Academic Editor Frederic Brunet

Copyright copy 2013 Kazuhiko OhshimaThis is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

A substantial number of ldquoretrogenesrdquo that are derived from the mRNA of various intron-containing genes have been reported Aclass ofmammalian retroposons long interspersed element-1 (LINE1 L1) has been shown to be involved in the reverse transcriptionof retrogenes (or processed pseudogenes) and non-autonomous short interspersed elements (SINEs) The 31015840-end sequences ofvarious SINEs originated froma corresponding LINEAs the 31015840-untranslated regions of several LINEs are essential for retropositionthese LINEs presumably require ldquostringentrdquo recognition of the 31015840-end sequence of the RNA template However the 31015840-ends ofmammalian L1s do not exhibit any similarity to SINEs except for the presence of 31015840-poly(A) repeats Since the 31015840-poly(A) repeatsof L1 and Alu SINE are critical for their retroposition L1 probably recognizes the poly(A) repeats thereby mobilizing not only AluSINE but also cytosolic mRNAMany flowering plants only harbor L1-clade LINEs and a significant number of SINEs with poly(A)repeats but no homology to the LINEs Moreover processed pseudogenes have also been found in flowering plants I propose thatthe ancestral L1-clade LINE in the common ancestor of green plants may have recognized a specific RNA template with stringentrecognition then becoming relaxed during the course of plant evolution

1 RNA-Mediated Gene Duplicationand Retroposons

11 Retrogenes and Processed Pseudogenes Gene duplicationis a fundamental process of gene evolution [1] There are twotypes of gene duplication direct duplication of genomicDNAand retropositional events [2ndash4] Processed pseudogenes(PPs) are reverse-transcribed intronless cDNA copies ofmRNA that have been reinserted into the genome (Figure 1)[5 6] they are especially abundant in mammalian genomes[7 8] PPs are not usually transcribed because they lack anexternal promoter therefore they have long been viewedas evolutionary dead ends with little biological relevanceHowever recent studies have unveiled a substantial numberof ldquoprocessed genesrdquo or ldquoretrogenesrdquo with novel functions thatare derived from the mRNA of various intron-containinggenes [9ndash12] Molecular biological studies showed that aclass of mammalian retroposons long interspersed element-1 (LINE1 L1) has been involved in the reverse transcriptionof nonautonomous retroposons such as PPs (retrogenes) andshort interspersed elements (SINEs) [13]

12 Retroposons Eukaryotic genomes generally contain anextraordinary number of retroposons such as long ter-minal repeat (LTR) retrotransposons LINEs or non-LTRretrotransposons and SINEs [6 14 15] LINEs have beencharacterized as autonomous retroposons bearing either oneor two open reading frames (ORFs) all LINEs encode areverse transcriptase (RT) and some but not all encodean apurinicapyrimidinic endonuclease a ribonuclease Handor putative nucleic-acid-binding motifs (Figure 2) Mostmembers of a LINE family are truncated at various positionsin their 51015840 regions constituting defective members of thefamily the lengths of which range from 100 to 1000 bp [13]

The Bombyx R2 LINE protein which has sequence-specific endonucleolytic and RT activity makes a specificnick in one of the DNA strands at the insertion site anduses the 31015840 hydroxyl group that is exposed by this nickto prime the reverse transcription of its RNA transcript[16] This mechanism is referred to as target DNA-primedreverse transcription (TPRT) The last 250 nucleotides thatcorrespond to the 31015840-untranslated region (UTR) of the R2transcript are critical for this reaction [17] Other LINEs such

2 International Journal of Evolutionary Biology

Gene Processed pseudogene

Transcription

mRNA

SplicingReverse transcriptionand insertion into the genome

Figure 1 Schematic representation of the formation of a processedpseudogene

LINERNA Pol II

ORF1 ORF2

SINEPol III

tRNA or7SLRNA 5SrRNA

ORF1 protein Endonuclease andreverse transcriptase

Figure 2 Schematic representation of a SINE and a LINE that havethe same 31015840-end sequence Three-dimensional protein structuresare taken from the L1-encoded ORF1 protein [94] and the reversetranscriptase of human immunodeficiency virus type 1 [95]

as L1 are also believed to retrotranspose by TPRT [18] Thehuman L1 TPRT machinery has been reconstructed in vitro[19]

SINEs are non-autonomous retroposons the 51015840-endsequences of which are derived from tRNA 5S rRNA or7SL RNA with promoter activity for RNA polymerase III(Figure 2) [20ndash22] On the other hand the 31015840-end sequencesof SINEs generally originated from a corresponding LINE[23] A small nucleolar RNA-derived short retroposon whichlacks internal promoters for RNA polymerase III and hastherefore not been subject to multiple rounds of retroposi-tion was recently discovered in the platypus [24]

13 Evolutionary Relationships of Various LINEs Eickbushrsquosgroup conducted comprehensive phylogenetic analysis ofLINEs using extended sequence alignment of their RTdomains [25] All identified LINEs were grouped into 11distinct clades Assuming vertical descent the phylogenysuggests that LINEs are as old as eukaryotes with eachof the 11 clades dating back approximately 2 billion years[25] Currently almost 30 clades have been recognized [26]Mammalian L1s belong to the L1 clade which includesnumerous LINEs from vertebrates slime mold plants andalgae [25 27 28] Analyses of L1-encoded endonucleases fromzebrafish and mammals revealed that they are divided into3 groups M F and Tx1 [29] Kordis et al showed that thegenomes of deuterostomes possess three highly divergentgroups of L1-clade LINEs which are distinct from Tx group[28] The Tx group with a target-specific insertion consistsof 2 branches one of which includes frog Tx1 [30]

14 SINEs and LINEs The31015840-end sequences of various SINEsoriginated from a corresponding LINE (Figure 2) [31] forreviews see also [23 32 33] A systematic database and liter-ature survey identified 58 SINEs each possessing a common31015840-end sequence with its partner LINE (Table 1) [34] Forexample Figure 3 shows the alignment of tobacco TS SINE[35] with its partner LINE This LINE which was recentlyidentified in the potato genome amember of the same familyas tobacco belongs to the RTE clade The 31015840-end sequenceof the SINE approximately 100 bases is nearly identical tothat of the LINE and they both end in TTG repeats [34]SINELINE pairs have been observed in a wide variety ofspecies from eumetazoans to green plants confirming thegenerality of this phenomenon (Table 1) Although variousLINEs appear in the list those from clades CR1 and RTEwereparticularly predominant

Since the R2 LINE protein specifically recognizes thesequence near the 31015840-end of the RNA transcript for the initi-ation of first-strand synthesis [16 17] the homology betweenthe 31015840-ends of SINEs and LINEs suggests that each SINEfamily recruits the enzymatic machinery for retropositionfrom the corresponding LINE through this common ldquotailrdquosequence [31] This hypothesis was strongly supported byexperiments with SINE sequences in the eel [36] As the 31015840-UTRs of several LINEs have been shown to be essential forretroposition [17 36ndash39] these LINEs presumably requireldquostringentrdquo recognition of the 31015840-end sequence of the RNAtemplate [32 36]

Figure 4 illustrates the relationship between the numberof SINELINE pairs and the number of LINEs in each clade[34] Although Spearmanrsquos rank correlation is not significant(120588 = 025) the number of SINEs with a LINE tail is positivelycorrelated with the number of LINEs belonging to each clade(1198772 = 083) that is more LINEs tend to lead to moreSINELINE pairs Therefore although a few LINE clades arethe predominant source of SINELINE pairs it is plausiblethat this simply reflects the large number of LINEs in theseclades However L1-clade LINEs are the only prominentexception to this Although over 800 L1-clade LINEs appearedin the database only 3 SINEs with L1 tails were found [34]suggesting that in general L1-clade LINEs are different fromother LINEs with regard to 31015840-end recognition

15 Mechanism of RNA-Mediated Gene Duplication in Mam-mals Mammalian PPs and retrogenes were probably mobi-lized by L1s because they end in poly(A) and have L1-typetarget site duplications they are inserted in L1-type endonu-clease cleavage sites [40ndash42] Molecular biological studieshave shown that mammalian L1-encoded proteins have beeninvolved in the reverse transcription of PPs [43 44] In thesame assay another class of autonomous retroposons LTRretrotransposons (retroviral-like elements) were unable toproduce similar PP-like structures [43]

The 31015840-end sequences of mammalian L1 LINEs do notexhibit any similarity to SINEs except for the presence of31015840-poly(A) repeats although these L1s are thought to havemediated the retroposition of mammalian SINEs such as pri-mateAlu and rodent B1 families [45ndash47] Since the 31015840-poly(A)

International Journal of Evolutionary Biology 3

Box A Box B

GACAAGAGGGGTTGCTCTGATGGTAAGCAACCTCCACTTCCAACCAAGAGGTTGTGAGTTCGAGTCACCCCAAGAGCAAGGTGGGGAGTT

TTTCTTGATTATTGCTCCTTGTTGTTAAATTTTGTATTGATGTTAGTTTTATTATTTTCTTCCTTTACTTGG

CTTGGAGGGAAGGATGCCGAGGGTCTATTGGAAACAGCCTCTCTACC-CCA--GGGTAGGGGTAAGGTCTGCGTACACACTACCCTCCCC

ATTTCTTGATTCCTCGATCT

AGACCCCAC-TAGTGGGATTATACTGGGT-TG (TTG)0minus14

CTCATTGTTGTTGTTG-3998400-3998400

TSRTE-1 STu

TSRTE-1 STu

TSRTE-1 STu 4095

207

4051177

396190

Figure 3 Sequence comparison of tobacco TS SINE with its partner LINE The entire sequence of the TS SINE was aligned with the 31015840-end sequence (sim200 nucleotides) of a potato RTE-clade LINE Dots and hyphens represent identical nucleotides and gaps respectively ThetRNA-related region of the SINE is underlined with the promoter sequences for RNA pol III (A amp B boxes) highlighted in red Nucleotidepositions are shown on the right

(a) RandI(b) R4(c) Tad1(d) Rex1

(e) Vingi(f) Crack(g) I

0

5

10

15

20

25

30

0 200 400 600 800

SIN

Es

LINEs

CR1L2

RTE

L1a

bc

d ef g

R2 = 08343

Figure 4 Relationship between the number of SINELINE pairsand the number of LINEs in each clade The vertical axis shows thenumber of SINEs with a LINE tail [34] The horizontal axis showsthe number of LINEs belonging to each clade The linear regressionline determined by the least squares approach is shown except forL1 1198772 indicates the coefficient of determination CR1-clade LINEs(580 families) and L2-clade LINEs (10 families) were summed dueto their confusing nomenclature

repeats of L1 and Alu are critical for their retroposition inthe HeLa cell line [46 48 49] L1 probably recognizes the31015840-poly(A) repeats Therefore while mammalian L1s do notrequire stringent recognition of the 31015840-end sequence of theRNA templates they are able to initiate reverse transcriptionin a more ldquorelaxedrdquo manner [32]

L1-encoded proteins are cis-acting that is L1 proteinspreferentially mobilize or interact with the RNA moleculethat encoded them [43 44] However L1 is also thought tomobilize SINE RNAs and cytosolic mRNAs by recognizingthe 31015840-poly(A) tail of the template RNAs in trans resulting

in enormous SINE amplification and PP formation [4350] Given that the L1 retropositional machinery acts in acis-manner Boeke [51] proposed the poly(A) connectionhypothesis to explain whyAlu RNA ismobilized by L1 at sucha high frequency

Schmitz et al discovered a novel class of retroposons thatlack poly(A) repeats in mammals Termed tailless retropseu-dogenes they are derived from truncated tRNAs and tRNA-related SINE RNAs [52] To explain this phenomenon theyproposed a novel variant mechanism probably guided by theL1 RT in which neither the presence of a poly(A) tail on theRNA template nor its length is important for retroposition

2 Retroposition Burst in Ancestral Primates

Abundant PPs are a feature of mammalian genomes [78] Previously my collaborators and I performed the firstcomprehensive analysis of human PPs using all knownhuman genes as queries [50] We found the possibility ofa nearly simultaneous burst of PP and Alu formation inthe genomes of ancestral primates The human genomewas queried and 3664 candidate PPs were identified themost abundant of which were copies of genes encodingkeratin 18 glyceraldehyde-3-phosphate dehydrogenase andribosomal protein L21 A simple method was developed toestimate the level of nucleotide substitutions (and thereforethe age) of the PPs A Poisson-like age distribution wasobtained with a mean age close to that of the Alu repeatsThese data suggested a nearly simultaneous burst of PPand Alu formation in the genomes of ancestral primatesSimilar results have been reported by other groups [53ndash55] The peak period of amplification of these 2 distinctretroposons was estimated to be 40ndash50 million years ago(mya) [50] moreover concordant amplification of certain L1subfamilies with PPs and Alus was observed We proposeda possible mechanism to explain these observations in whichthe proteins encoded bymembers of particular L1 subfamiliesacquired an enhanced ability to recognize cytosolic RNAs intrans

Roy-Engelrsquos group recently recreated and evaluated theretroposition capabilities of two ancestral L1 elements L1PA4and L1PA8 which were active sim18 and sim40 mya respectively[56] Relative to the modern L1PA1 subfamily they found


Table 1 Identification of SINELINE pairs [34]

SINE Species Promoter LINE tail Description ofSINELINE pair

MammalsMIR (CORE-SINEsTher-1 Mon-1) [97ndash99] All mammals tRNA L2 [15] [100]

CORE-SINEs (MIR3Ther-2) [15 99] Mammals tRNA L3 [101] [15 34 102]CORE-SINEs(Mar-1MAR1 MD) [15 99] Marsupials tRNA RTE-3 MD [15] [15 34 102]

MAR4(MAR4 MD WALLSI3) [15]

Opossum and wallabyMonodelphis domestica

Macropus eugenii(51015840-end of RTE) RTE-2 (MD ME) [15] [15 34]

RTESINE1 [15] OpossumMonodelphis domestica (51015840-end of RTE) RTE-1 MD [15] [34]

Ped-1 [103] SpringharePedetes capensis (Rodentia) 5S rRNA BovB Pca [103] [103]

Ped-2 [103] SpringharePedetes capensis (Rodentia) tRNA (ID SINE) BovB Pca [103] [103]

Bov-tA [104 105] Ruminants tRNAGlu Bov-B [105 106] [100 104]Bov-A2 [104 105] Ruminants (51015840-end of BovB) Bov-B [105 106] [104]SINE2-1 EC [15] Horse Equus caballus tRNA RTE-1 EC [15] [15 34]Afro SINEs(AFRO LA PSINE1) [15 107] All Afrotherians tRNA RTE1 (LA Pca) [15] [34 103 108]

RTE1-N1 LA [15] ElephantLoxodonta africana (51015840-end of RTE) RTE1 LA [15] [15]

SINE2-1 Pca [15] Hyrax Procavia capensis tRNA RTE1 Pca [15] [15]Birds and Reptiles

TguSINE1 [15] Zebra finchTaeniopygia guttata tRNAIle CR1-X [15] [15]

Tortoise Pol IIISINE [31 109ndash111] Tortoises and turtlesCryptodira tRNALys PsCR1 [112] [31 113]

Sauria SINE [114 115] Lizard Anolis carolinensis tRNA Anolis Bov-B [114] [114]Anolis SINE 2 [115] Lizard Anolis carolinensis (Box A amp B) Anolis LINE 2 [115] [115]SINE2-1B AcarSINE2-1 Acar [15] Lizard Anolis carolinensis tRNA Vingi-2 Acar [116] [15 34]

Amphibians

V-SINEs (SINE2-1 XT) [15] Frog Xenopus (Silurana)tropicalis tRNA L2-4 XT

(L2-3 L2-6 L2-2) [15] [15 34]

CORE-SINEs (MIR Xt) [15] Frog Xenopus (Silurana)tropicalis tRNA L2-5 XT [15] [34]

Fish

Sma I [117 118] Chum and pink salmonOncorhynchus tRNALys SalL2 [23] [23 31 32]

Fok I [118] Charr Salvelinus tRNALys SalL2 [23] [23 31 32]SlmI [119] All salmonids Salmonidae tRNALeu RSg-1 [120] [119]CORE-SINEs (Hpa I) [102 118] All salmonids Salmonidae tRNA RSg-1 [120] [31]CORE-SINEs(AFC SINE2-1 AFC) [102 121 122] Cichlid fish Cichlidae tRNA CiLINE2 [121] [121]

CORE-SINEs(UnaSINE1 UnaSINE2) [123] Eel Anguilla japonica tRNA UnaL2 [36 123] [36 123]

HAmo SINE [124] Carp Cyprinidae tRNA HAmoL2 [124] [124]


Table 1 Continued


DeuSINEs(AmnSINE1 SINE3) [21 125] Mammals chicken

zebrafish catfish 5S rRNA CR1-4 DR (CR1-7CR1-9 CR1-13) [15] [21 34 125]

DeuSINEs(LmeSINE1 SacSINE1) [125]

Coelacanth and dogfishshark

Latimeria menadoensisSqualus acanthias

tRNA CR1-4 DR-like [15] [125]

DeuSINEs (OS-SINE1) [119 125] Salmon and troutOncorhynchus Salmo 5S rRNA RSg-1 [120] [125]

V-SINEs (HE1) [126 127]Sharks and rays

M manazo S torazameH japonicus T californica

tRNA HER1 [126] [126]

V-SINEs (DANA) [127ndash129] Zebrafish Danio rerio tRNA CR1-3DRZfL3 [15 127] [127]

V-SINEs (Lun1) [127] LungfishLepidosiren paradoxa tRNA LfR1 [127] [127]

SINEX-1 CMSINE2-1 CM [130] Elephant sharkCallorhinchus milii tRNA CR1-2 CM DQ524334 [34 130]

Chordates

DeuSINEs (BflSINE1) [125] AmphioxusBranchiostoma floridae tRNA Crack-16 BF [15] [34]

Deuterostomes

SURF1SINE2-4c SP [15 131]Sea urchin

Strongylocentrotuspurpuratus

tRNA CR1-4 SP [15] [34]

DeuSINEs (SINE2-3 SP) [15 125]Sea urchin


tRNA CR1Y SP(CR1X SP) [15] [15 34]

SINE2-8 SP(SINE2-6 SINE2-4b) [15]

Sea urchinStrongylocentrotus

purpuratustRNA L2-1 SPCR1-3 SP [15] [34]

Protostomes

Gecko [132] Mosquito Aedes aegypti tRNA

I-74 AAe (MosquII-58 I-59 I-62

I-64I Ele10 14 35 37)

[15 133] [34 132]

Eumetazoans

Nve-Nin-DC-SINE-1 (lowast1) [134] Sea anemoneNematostella vectensis tRNA L2-22 NV [15] [134]

Nve-Nin-DC-SINE-2 (lowast1) [134] Sea anemoneNematostella vectensis tRNA CR1-5 NV [15] [134]


SINE2-1 NV [15] Sea anemoneNematostella vectensis tRNA CR1-16 NV [15] [34]

SINE2-5 NV [15] Sea anemoneNematostella vectensis tRNA Rex1-24 NV [15] [34]

Fungi

Mg-SINE [135] Rice blast fungusMagnaporthe grisea tRNA MgLMGR583 AF018033 [32 34]

SINE2-1 BG [15] Powdery mildew fungusBlumeria graminis tRNA Tad1-24 BG

(HaTad1-3 1-5) [15] [34]


Table 1 Continued


AmoebozoaEdSINE1 (SINE-lile) [136] Amoeba Entamoeba dispar Unknown R4-1 ED [15] [34]R4-N1 ED (SINE-lile) [15] Amoeba Entamoeba dispar Unknown R4-1 ED [15] [34]

EhLSINE1ehapt2 (SINE-lile) [137 138] AmoebaEntamoeba histolytica Unknown EhLINE1EhRLE1 [30 137] [137]

EhLSINE2 (SINE-like) [137] AmoebaEntamoeba histolytica Unknown EhLINE2EhRLE3 [30 137] [137]

Land plants

TS [35] TobaccoNicotiana tabacum tRNA RTE-1 Stu [15] [34]

ZmSINE2SINE2 SBi [66] Maize Zea maysSorghum Sorghum bicolor tRNA LINE1-1 ZM [15] [34 66]

ZmSINE3 [66] Maize Zea mays tRNA LINE1-1 ZM [15] [66]Green algae

SINEX-1 CR [15 83] Chlamydomonas reinhardtii Unknown RandI-2DualenCr3 [15 139] [34 83]

SINEX-2 CR [15 83] Chlamydomonas reinhardtii Unknown RandI-2 (RandI-3) [15 139] [83]SINEX-3 CR [15 83] Chlamydomonas reinhardtii tRNA L1-1 CR [15] [15 83]SINEX-4 CR [15 83] Chlamydomonas reinhardtii Unknown RandI-2 (RandI-3) [15 139] [34 83]SINEX-5 CRSINEX-6 CR [83] Chlamydomonas reinhardtii tRNA RandI-5 [15] [83](lowast1) Subfamilies

that both elements were similarly active in a cell cultureretroposition assay in the HeLa cell line and both wereable to efficiently trans-mobilize Alu elements from severalsubfamilies They found limited evidence of differentialassociations between Alu and L1 subfamilies suggestingthat other factors are likely the primary mediators of theirchanging interactions over evolutionary time Populationdynamics and stochastic variation in the number of activesource elements likely played an important role in individualLINE or SINE subfamily amplification [56] If coevolutionalso contributed to changing retroposition rates and theprogression of subfamilies cell factors were likely to play animportant mediating role in changing LINE-SINE interac-tions over evolutionary time

We hypothesized that many human retrogenes werecreated during this period and that such retrogenes wereinvolved in generating new characteristics specific to simianprimates [50] Several intriguing examples of primate retro-genes have been reported for example the human brain-specific isotype of the glutamate dehydrogenase (GLUD2)gene [57] the brain- and testis-specific CDC14Bretro genewhich evolved from the CDC14B cell cycle gene [58] anda novel chimeric retrogene (PIPSL) created by a uniquemechanism [59ndash61] emerged by retroposition in a hominoidancestor [54 55 62ndash65]

3 A Primate Retrogene That Was Created bya Novel Mechanism

31 Gene Creation by the Coupling of Gene Duplication andDomain Assembly Most new genes arise by the duplicationof existing gene structures after which relaxed selection onthe new copy frequently leads to mutational inactivation of

the duplicate only rarely will a new gene with a modifiedfunction emerge My collaborators and I described a uniquemechanism of gene creation whereby new combinations offunctional domains are assembled at the RNA level fromdistinct genes and the resulting chimera is then reverse-transcribed and integrated into the genome by the L1retrotransposon [59] We characterized a novel gene whichwe termed PIP5K1A and PSMD4-like (PIPSL) created bythis mechanism from an intergenic transcript between thephosphatidylinositol-4-phosphate 5-kinase (PIP5K1A) andthe 26S proteasome subunit (PSMD4) genes in a homi-noid ancestor PIPSL is transcribed specifically in the testisof humans and chimpanzees and is posttranscriptionallyrepressed by independent mechanisms in these primate lin-eagesThe PIPSL gene encodes a chimeric protein combiningthe lipid kinase domain of PIP5K1A and the ubiquitin-bindingmotifs of PSMD4 Strong positive selection on PIPSLled to its rapid divergence from the parental genes forminga chimeric protein with distinct cellular localization andminimal lipid kinase activity but significant affinity for cel-lular ubiquitinated proteins [59] PIPSL is a tightly regulatedtestis-specific novel ubiquitin-binding protein formed by anunusual exon-shuffling mechanism in hominoid primatesand represents a key example of the rapid evolution of a testis-specific gene

32 Evolutionary Fate of Primate PIPSL Domain shufflinghas provided extraordinarily diverse functions to proteinsnevertheless how newly combined domains are coordinatedto create novel functions remains a fundamental question ofgenetic and phenotypic evolution My group presented thefirst evidence for the translation of PIPSL in humans [61]Thehuman PIPSL locus showed low nucleotide diversity within 11


Table 2 31015840-Repeats of plant SINE families [34]

SINE Species 31015840-Repeat LINE tail Reference for SINEsGreen algae

SINEX-1 CR Chlamydomonas reinhardtii (ATT)119899 RandI-2DualenCr3 [83]SINEX-2 CR Chlamydomonas reinhardtii (CTTT)119899 RandI-2 (RandI-3) [83]SINEX-3 CR Chlamydomonas reinhardtii (A)119899 L1-1 CR [83]SINEX-4 CR Chlamydomonas reinhardtii (ATT)119899 RandI-2 (RandI-3) [83]SINEX-5 CRSINEX-6 CR Chlamydomonas reinhardtii (ATT)119899 RandI-5 [83]

Seed plantsAu Angiosperms and a gymnosperm (T)2ndash5 Nd [76ndash79]ZmSINE1 (Au-like) Zea mays (T)119899 Nd [66]SINE2-1 ZM (Au-like) Zea mays (T)3 Nd [15]SINE-5 Mad (Au-like) Malus x domestica (T)3 Nd [15]

Monocotsp-SINE1 Oryza sativa (T)119899 Nd [74]p-SINE2 Oryza sativa (T)119899 Nd [75]p-SINE3 Oryza sativa (T)119899 Nd [75]ZmSINE21lowastSINE2-1a SBi Zea mays Sorghum bicolor (T)119899 LINE1-1 ZM [15 66]ZmSINE22lowast Zea mays (T)119899 LINE1-1 ZM [66]ZmSINE23lowast Zea mays (T)119899 LINE1-1 ZM [66]SINE2-1 SBi (ZmSINE2-like) Sorghum bicolor (T)119899 LINE1-1 ZM [15]SINE2-1c SBi (ZmSINE2-like) Sorghum bicolor (T)119899 LINE1-1 ZM [15]ZmSINE3 Zea mays (A)119899 LINE1-1 ZM [66]OsSN1F524 Oryza sativa (A)119899 Nd [140]OsSN2SINE2-12 SBi Oryza sativa Sorghum bicolor (A)119899 Nd [15 140]OsSN3 Oryza sativa (A)119899 Nd [140]SINE9 OSSINE2-11 SBi (OsSN-like) Oryza sativa Sorghum bicolor (A)119899 Nd [15]

EudicotsTS Nicotiana tabacum (TTG)119899 RTE-1 STu [35]SB1-15 (S1AtSNRAthEBoS) Arabidopsis thaliana Brassicaceae (Cruciferae) (A)119899 Nd [68 69 141ndash144]LJ SINE-1 Lotus japonicus (A)119899 Nd [145]LJ SINE-2 Lotus japonicus (A)119899 Nd [145]LJ SINE-3 Lotus japonicus (A)119899 Nd [145]MT SINE-1 Medicago truncatula (A)119899 Nd [145]MT SINE-2 Medicago truncatula (A)119899 Nd [145]MT SINE-3 Medicago truncatula (A)119899 Nd [145]SINE-1 Mad Malus x domestica (A)119899 Nd [15]SINE-2 Mad Malus x domestica (A)119899 Nd [15]SINE-4 Mad Malus x domestica (A)119899 Nd [15]SINE2-1 PTr Populus trichocarpa (A)119899 Nd [15]SINE2-2 PTr Populus trichocarpa (A)119899 Nd [15]lowast

subfamilies Nd no data

populations (125 individuals) compared with other genomicregions such as introns and overall chromosomes It wasequivalent to the average for the coding sequences or exonsfrom other genes suggesting that human PIPSL has somefunction and is conserved among modern populations Twolinked amino acid-altering single-nucleotide polymorphismswere found in the PIPSL kinase domain of non-African pop-ulations They are positioned in the vicinity of the substrate-binding cavity of the parental PIP5K1A protein and changethe charge of both residues The relatively rapid expansion of

this haplotype might indicate a selective advantage for it inmodern humans [61]

We determined the evolutionary fate of PIPSL domainscreated by domain shuffling [61] During hominoid diver-sification the S5aPSMD4-derived domain was retained inall lineages whereas ubiquitin-interacting motif (UIM) 1 inthe domain experienced critical amino acid replacementsat an early stage being conserved under subsequent highlevels of nonsynonymous substitutions to UIM2 and otherdomains suggesting that adaptive evolution diversified these


Table 3 31015840-Repeats of plant LINE families [34]

Species LINE clade Families 31015840-Repeat(A)119899 Other repeats None

Flowering plants L1 233 224 0 9RTE 7 0 7

lowastb 0L1 15 2

lowasta8lowastc 5

Green algae RandI 8 0 8lowastd 0

RTEX 6 0 6lowaste 0

lowastaL1-1 CR (Chlamydomonas) Zepp (Chlorella)lowastb(TTG)119899 (TTGATG)119899lowastc(CATA)119899 (CA)119899 (CAA)119899 (TAA)119899lowastd(ATT)119899 (CTATTT)119899lowaste(CA)119899 (CAA)119899 (CCAT)119899 (ACAATG)119899 (CTTGTAA)119899

functional compartments (Figure 5) [61] Conversely thePIP5K1A-derived domain is degenerated in gibbons andgorillas These observations provide a possible scheme ofdomain shuffling in which the combined parental domainsare not tightly linked in the novel chimeric protein allowingfor changes in their functional roles leading to their fine-tuning Selective pressure toward a novel function initiallyacted on one domain whereas the other experienced a nearlyneutral state Over time the latter also gained a new functionor was degenerated

4 RNA-Mediated Gene Duplication inLand Plants

The SINELINE relationship in land plants is controversialThe first SINELINE pair of land plants was reported recentlyin maize [66] However the three tRNA-derived SINE fam-ilies in Arabidopsis thaliana do not exhibit any similarityto the only LINE family (ATLN) in its genome [67ndash69]Deragonrsquos group proposed that the SINE-LINE relationshipin Arabidopsis is not based on primary sequence identity buton the presence of a common poly(A) region [68]

I systematically analyzed the increasing wealth ofgenomic data to elucidate the SINELINE relationships ineukaryotic genomes especially plants [34] I proposed thatthe ancestral L1-clade LINE in the common ancestor of greenplants may have used stringent RNA recognition to initiatereverse transcription During the course of plant evolutionspecific recognition of the RNA template may have been lostin a plant L1 lineage as in mammals

41 L1-Clade LINEs Are Predominant in the Genomes ofFlowering Plants Figure 6 represents the number of LINEsbelonging to each LINE clade according to biological taxa[34] The L1 clade is the largest of all the clades with L1-clade LINEs being predominant in mammals and land plants(mainly flowering plants) The genomes of flowering plantsharbor almost exclusively L1-clade LINEs (RTE-clade LINEsare also found in several species)

While a significant number of SINEs more than halfof which end in poly(A) repeats have been identified inthe genomes of flowering plants (Table 2) [34] only three

SINELINE pairs have been discovered in their genomes thatis maize ZmSINE2 and ZmSINE3 [66] and tobacco TS SINE[34] Interestingly many PPs have been reported in floweringplants [11 70ndash73] Since mammalian L1s are thought torecognize the 31015840-poly(A) tail of RNA when forming PPs [43]it is possible that the plant LINE machinery is similar tothat of mammalian L1s [68] that is plant L1-clade LINEspresumably recognize the 31015840-poly(A) tail of RNA therebymobilizing SINEs with a poly(A) tail and mRNA

In accordance with this hypothesis almost all L1-cladeLINEs in flowering plants end in poly(A) repeats while allRTE-clade LINEs end in (TTG)n or (TTGATG)n (Table 3)[34] As for the exceptional cases of p-SINEs [74 75] andAu-like SINEs [76ndash79] which end in poly(T) tracts (or ashort stretch of T) it is possible that they are mobilized byunidentified partner LINEs that recognize a poly(U) repeatof RNA at the 31015840-terminus

42 Plant L1-Clade LINEs Consist of 3 Deeply Branching Lin-eages That Have Descended from the Common Ancestor ofMonocots and Eudicots Comprehensive phylogenetic analy-sis of L1-clade LINEs revealed three important points [34]First L1-clade LINEs from distinct taxa (ie land plantsgreen algae and vertebrates) formed monophyletic groupsStatistical support for the monophyly of land plants andgreen algae was high with bootstrap values of 10082 and9783 (NJML methods) respectively The monophyly ofvertebrate F and M lineages was not supported by theML method Second the L1 lineages from these three taxaformed a monophyletic group (5545 NJML methods)among diverged LINE clades such as RTE and CR1 The Tx1LINE with a target-specific insertion was also found in thisclade as observed in previous studies [26 29 30] The Tx1and vertebrate F lineage formed a monophyletic group withhigh confidence (9485)Third comparisonwith species phy-logeny revealed that plant L1-clade LINEs consist of at leastthree deeply branching lineages that have descended fromthe common ancestor of monocots and eudicots (ME1ndash3)These 3 lineages must have arisen more than 130 mya whichis the approximate divergence ofmonocots and eudicots [80]The history of plant L1 lineages is therefore reminiscent ofthat of vertebrate L1-clade LINEs which are divided into


Human PIPSL

Chimp PIPSL

Gorilla PIPSL

Orang PIPSL

Gibbon PIPSL

Human

Chimpanzee

Orangutan

Macaque

Cow

Dog

Mouse

PIP5K

0 21

005 S5a

30 10

102 73

168 20

71 10

0 00 56

41 4161 061 6251 11

10 0

0 4116 241

10 310 11

10 93

36 548

14 5680 133

137 956

Figure 5 Molecular phylogeny and pattern of nucleotide substitutions of the S5a-derived region of PIPSL from all hominoid lineages [61]The branches are drawn in proportion to the number of substitutions with nonsynonymous (n) and synonymous (s) substitutions shownabove each branch (n s) An ancestral PIPSL lineage (indicated by bold lines) gradually accumulated 19 nonsynonymous and 2 synonymoussubstitutions Since the split from the ancestral lineage all the respective lineages have accumulated synonymous substitutions except forgibbons which still have a high n s ratio (17 2)

050

100150200250300350400

R4 L1

RTE

CR1

and

L2

Rex1

Crac

k

Ving

i I

Oth

ers

Mammals ArthropodsLand plantsNonmammalian

vertebrates

Figure 6 The number of LINE families belonging to each LINEclade according to biological taxa [34] LINE clades in which thepartner LINE of a SINE was identified are shown The remainingclades are grouped as ldquoOthersrdquo (Repbase 1610) land plants mostlyflowering plants

several ancestral lineages (M and FTx1) one of which leadsto mammalian L1s [28 29]

43 A Conserved 31015840-End Sequence with a Solid RNA Structureas in Maize and Sorghum SINEs Observed in One PlantL1 Lineage One monocot L1 lineage (monocot 1a in ME1)consisted of a large number of L1-clade LINEs that wereidentified mainly in the recently released maize and sorghum

genomes Moreover one group of LINEs in this lineageretained a conserved 31015840-end sequence [34] The averagepairwise divergence of this region (the last 45 nucleotides)among the LINEs was only 0144 (standard error (SE) 0043)whereas that for the entire sequence was 0570 (SE 0012)Interestingly maize SINEs (ZmSINE2 and ZmSINE3) with31015840-end sequences very similar to that of a LINE belongingto this group LINE1-1 ZM were reported recently [66] Ifurther revealed that several sorghum SINEs also possesssimilar 31015840-end sequences [34] Comparisons of the 31015840-endsequences from these SINEs and LINEs revealed that partof the sequence (sim50 nucleotides) is apparently relatedpresumably they were derived from a common ancestral L1sequence (Figure 7) [34]

Furthermore the putative transcript from this regionforms a putative hairpin structure (Figure 8) [34] Com-pensatory mutations were observed in the stem-formingsequences confirming a secondary structure Several nucle-otides were strongly conserved in the 31015840-flanking region ofthe stem (51015840-CGAG-31015840) and in the loop (51015840-UCU-31015840) thoughthe stem-forming nucleotides were variable This stem-loopstructure is commonly observed in the 31015840-end sequences ofLINEs and SINEs of the stringent type [38 81 82] Theseresults strongly suggest that at least in this lineage plantLINEs require a particular 31015840-end sequence of the stringenttype

44 Origin of Stringent and Relaxed 31015840-End Recognition ofPlant L1-Clade LINEs The last example of a SINELINE pair


|||||||||||||| || ||| ||||| ||||||| |

| || || ||||| ||| || || | || || | |

| ||||| || |||||| |||||||||||||||

CTATTTTAGACCTTTTTTTCT-CTTCTYTTAATATAATG---ATACGCAG---CTCTCCTGCGTGTTCGAGAAAAAAAAA-3998400

CTATTTTAGACCTTATTATCTCCTTCT--TAATATATTT--AAGGCGCAG---TTCCCCTGCGCTTTCGAGAAAAAAAAAA-3998400|||||| ||| |||||

GGCCTGGGTGAGAAGGTACCTTCTTCT--TAATAYAATRCCCGGGGGCNGTCTTWCCCCTCCSCGGTCGAGTTT-3998400

Monocot 1a

LINE1-1 ZM

SINE2 consensus

Figure 7 Sequence comparisons of the 31015840-end sequences of L1-clade LINEs andmonocot SINE familiesThe 31015840-end sequences of themonocot1a (consensus) LINE1-1 ZM and SINE2 (consensus) were aligned [34] Vertical lines and hyphens represent identical nucleotides and gapsrespectively A conserved region between the LINEs and SINEs is boxed R AG Y CT S CG WAT N any nucleotide

UCCC

C

C

C

CC

U

UG

GG

G

G

GGG

A

UUUUUU U

AAAAAA

UUA

A

L1 consensus(monocot 1a)

12

C CC

C

CC

C

CC

UU

UG

GG

G

GG

GG

A

UU

U

UUU UU UAAAAAA A

12

UU

C C

C

C

C

G

GCG

G

C

C

GCG

GGGGG

G

UA

U

UU U

A

AA AA A

U

A

LINE1-1 ZM

ZmSINE3 ZmSINE22 ZmSINE23CC

C

CC

G

GC

CC

CC C C

GG

G

GG G G

G

GG

U

U

UUUUU

U

UU

U

A

AAAAAA A

3

4

CC

C

CC

C

G

G

CC

CC C C

G

GCG

GG G G

G

GG

U

UUUUU

U

UU

U

A

AAAAAA A

C

C CC

CC

CGCGC

C

C

G

G

GCG

G

GG

GGGG

UUU

AAA

CC

C

G

G UUU

CAU

UU UU AA A

U

A

5

SINE2-1 SBi

C

C

GCG

CGC

CC

GG

C GC

CG

GGG UUU AAAA

A

CC

G

C GA

A

5

UU A

ZmSINE21SINE2-1a SBi

C

C C

GCG

CG

CG

CC

G

C

C

G

G

GGG

UG U

U

UUU AA A AUU A

CGG

SINE2-1c SBi

3

4

Figure 8 Secondary structure models for the 31015840-end sequences of L1s and monocot SINEs The putative transcripts form putative hairpinstructures Compensatory mutations (1ndash5) are shown by red rectangles Conserved nucleotides are indicated by blue circles The minimumfree energy levels were minus108 or minus126 (kcalmol) for L1s (monocot 1a and LINE1-1 resp) and (minus125)ndash(minus137) for SINEs (ZmSINE23 minus154and SINE2-1c minus177) The structures were deduced using mfold [96]

in the L1-cladewas found in a green algaThe 31015840-end sequence(sim80 nucleotides) of Chlamydomonas SINEX-3 CR [83] wasvery similar to that of L1-1 CR both ending in poly(A) repeats[34] Since land plants emerged from green algae [84] thefollowing mechanism is proposed for the 31015840-end recognitionof plant L1-clade LINEs (Figure 9)

It is possible that the ancestral L1-clade LINE in thegenome of the common ancestor of green plants possessedstringent nonmammalian-type RNA recognition propertiesDuring the course of plant evolution an L1 lineage thenlost the ability to recognize specifically the RNA templatefor reverse transcription thereby introducing relaxed 31015840-end


ME1

ME2

ME3

M

F

MonocotsEudicots

MammalsFishes

Loss

Loss

Stringent

Green algae

MonocotsEudicots

MonocotsEudicots

Fishes

Figure 9 Proposed model for the 31015840-end recognition of L1-clade LINEs The ancestral L1-clade LINE in the ancestral greenplant possessed a stringent nonmammalian-type RNA recognitionproperty During the course of plant evolution an L1 lineage lostthe ability to recognize specifically the RNA template for reversetranscription thereby introducing relaxed 31015840-end recognition inland plants ME1ndash3 plant L1 lineages M F vertebrate L1 lineages

recognition in land (flowering) plants as well as in mammalsThis model assumes that rigid sequence specificity was anancestral state although the timing of its loss might besubject to debate Since horizontal transfer of LINEs betweeneukaryotes is rare [25 85ndash87] the discontinuous distributionof L1-clade LINEs with low specificity (ie mammalian L1sand plant ME2ME3) suggests a type of parallel evolution

The ancestral L1-clade LINE might have required the 31015840-end sequence and the terminal poly(A) repeats A few L1lineages might then have lost their specific interaction withthe 31015840-UTR of the template RNA retaining some role for the31015840-repeats As shown in Table 3 most plant L1-clade LINEsas well as mammalian L1s have poly(A) repeats at their31015840-termini however 31015840-poly(A) repeats are not necessarilya hallmark of relaxed 31015840-end recognition For examplealthough silkworm SART1 an R1-clade LINE uses stringent-type recognition (its 31015840-UTR is essential for retroposition)it ends in poly(A) repeats [37 38] which are necessary forefficient and accurate retroposition [38] Other LINEs endin repeating units other than poly(A) for example the Ielement (I clade) ends in TAA repeats [88] while UnaL2 (L2)ends in TGTAA repeats which are likely involved in templateslippage during reverse transcription [36]

Alternatively the ancestral L1-clade LINE may have pos-sessed relaxed mammalian-type RNA recognition proper-ties During the course of plant evolution the L1 lineagesof land plants (ME1) and green algae might then havegained specific stringent-type recognition of the RNA tem-plate However it is difficult to imagine that the molecularmachinery for rigid sequence specificity such as the partic-ular conformation of the RNA-binding domain has arisenindependently under reduced constraints

In vivo retroposition assays have been developed forseveral LINEs [36 37 39 48] Using such systems it willbe possible to verify these 2 models by evaluating the

dispensability of the 31015840-end sequence or poly(A) repeats innewly characterized L1 lineages such as plant ME1 and fish F

5 Concluding Remarks

L1 LINEs have contributed significantly to the architectureand evolution of mammalian genomes whereas LTR retro-transposons are overwhelmingly found in certain floweringplants Understanding the independent origins of flexible 31015840-end recognition may help us to determine what distinguishesthe fate of a retroposon in the eukaryotic genome and why ithas succeeded so well in certain genomes [89ndash93]

Acknowledgment

This work was supported by an institutional grant from theNagahama Institute of Bio-Science and Technology to KOhshima

References

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[2] M Long E Betran K Thornton and W Wang ldquoThe origin ofnew genes glimpses from the young and oldrdquo Nature ReviewsGenetics vol 4 no 11 pp 865ndash875 2003

[3] D V Babushok EMOstertag andHH Kazazian Jr ldquoCurrenttopics in genome evolutionmolecularmechanisms of new geneformationrdquo Cellular and Molecular Life Sciences vol 64 no 5pp 542ndash554 2007

[4] C Charon Q Bruggeman V Thareau and Y Henry ldquoGeneduplication within the green lineage the case of TEL genesrdquoJournal of Experimental Botany vol 63 no 14 pp 5061ndash50772012

[5] E F Vanin ldquoProcessed pseudogenes characteristics and evolu-tionrdquo Annual Review of Genetics vol 19 pp 253ndash272 1985

[6] A M Weiner P L Deininger and A Efstratiadis ldquoNonviralretroposons genes pseudogenes and transposable elementsgenerated by the reverse flow of genetic informationrdquo AnnualReview of Biochemistry vol 55 pp 631ndash661 1986

[7] Z Yu D Morais M Ivanga and P M Harrison ldquoAnalysis ofthe role of retrotransposition in gene evolution in vertebratesrdquoBMC Bioinformatics vol 8 article 308 2007

[8] Y-J Liu D Zheng S Balasubramanian et al ldquoComprehensiveanalysis of the pseudogenes of glycolytic enzymes in verte-brates the anomalously high number of GAPDH pseudogeneshighlights a recent burst of retrotrans-positional activityrdquo BMCGenomics vol 10 article 480 2009

[9] J Brosius ldquoRNAs from all categories generate retrosequencesthat may be exapted as novel genes or regulatory elementsrdquoGene vol 238 no 1 pp 115ndash134 1999

[10] H Kaessmann N Vinckenbosch and M Long ldquoRNA-based gene duplication mechanistic and evolutionary insightsrdquoNature Reviews Genetics vol 10 no 1 pp 19ndash31 2009

[11] H Sakai H Mizuno Y Kawahara et al ldquoRetrogenes in rice(Oryza sativaL ssp japonica) exhibit correlated expressionwiththeir source genesrdquo Genome Biology and Evolution vol 3 no 1pp 1357ndash1368 2011

[12] J Ciomborowska W Rosikiewicz D Szklarczyk WMakałowski and I Makałowska ldquoldquoOrphanrdquo retrogenes in


the human genomerdquo Molecular Biology and Evolution vol 30no 2 pp 384ndash396 2013

[13] H H Kazazian Jr ldquoMobile elements drivers of genomeevolutionrdquo Science vol 303 no 5664 pp 1626ndash1632 2004

[14] J Brosius ldquoRetroposonsmdashseeds of evolutionrdquo Science vol 251no 4995 p 753 1991

[15] J Jurka V V Kapitonov A Pavlicek P Klonowski O Kohanyand J Walichiewicz ldquoRepbase Update a database of eukaryoticrepetitive elementsrdquo Cytogenetic and Genome Research vol 110no 1ndash4 pp 462ndash467 2005

[16] D D Luan M H Korman J L Jakubczak and T H EickbushldquoReverse transcription of R2Bm RNA is primed by a nickat the chromosomal target site a mechanism for non-LTRretrotranspositionrdquo Cell vol 72 no 4 pp 595ndash605 1993

[17] D D Luan andTH Eickbush ldquoRNA template requirements fortarget DNA-primed reverse transcription by the R2 retrotrans-posable elementrdquo Molecular and Cellular Biology vol 15 no 7pp 3882ndash3891 1995

[18] J L Goodier and H H Kazazian Jr ldquoRetrotransposons revis-ited the restraint and rehabilitation of parasitesrdquo Cell vol 135no 1 pp 23ndash35 2008

[19] G J Cost Q Feng A Jacquier and J D Boeke ldquoHumanL1 element target-primed reverse transcription in vitrordquo TheEMBO Journal vol 21 no 21 pp 5899ndash5910 2002

[20] N Okada ldquoSINEs short interspersed repeated elements of theeukaryotic genomerdquo Trends in Ecology and Evolution vol 6 no11 pp 358ndash361 1991

[21] V V Kapitonov and J Jurka ldquoA novel class of SINE elementsderived from 5S rRNArdquo Molecular Biology and Evolution vol20 no 5 pp 694ndash702 2003

[22] N S Vassetzky and D A Kramerov ldquoSINEBase a database andtool for SINE analysisrdquoNucleic Acids Research vol 41 pp D83ndashD89 2013

[23] K Ohshima and N Okada ldquoSINEs and LINEs symbiontsof eukaryotic genomes with a common tailrdquo Cytogenetic andGenome Research vol 110 no 1ndash4 pp 475ndash490 2005

[24] J Schmitz A Zemann G Churakov et al ldquoRetroposedSNOfallmdasha mammalian-wide comparison of platypus snoR-NAsrdquo Genome Research vol 18 no 6 pp 1005ndash1010 2008

[25] H S Malik W D Burke and T H Eickbush ldquoThe age andevolution of non-LTR retrotransposable elementsrdquo MolecularBiology and Evolution vol 16 no 6 pp 793ndash805 1999

[26] V V Kapitonov S Tempel and J Jurka ldquoSimple and fastclassification of non-LTR retrotransposons based on phylogenyof their RT domain protein sequencesrdquoGene vol 448 no 2 pp207ndash213 2009

[27] A V Furano D D Duvernell and S Boissinot ldquoL1 (LINE-1)retrotransposon diversity differs dramatically between mam-mals and fishrdquo Trends in Genetics vol 20 no 1 pp 9ndash14 2004

[28] D Kordis N Lovsin and F Gubensek ldquoPhylogenomic analysisof the L1 retrotransposons in Deuterostomiardquo Systematic Biol-ogy vol 55 no 6 pp 886ndash901 2006

[29] K Ichiyanagi H Nishihara D D Duvernell and N OkadaldquoAcquisition of endonuclease specificity during evolution of L1retrotransposonrdquo Molecular Biology and Evolution vol 24 no9 pp 2009ndash2015 2007

[30] K K Kojima and H Fujiwara ldquoCross-genome screening ofnovel sequence-specific Non-LTR retrotransposons variousmulticopy RNA genes and microsatellites are selected as tar-getsrdquoMolecular Biology and Evolution vol 21 no 2 pp 207ndash2172004

[31] K Ohshima M Hamada Y Terai and N Okada ldquoThe 31015840ends of tRNA-derived short interspersed repetitive elementsare derived from the 31015840 ends of long interspersed repetitiveelementsrdquo Molecular and Cellular Biology vol 16 no 7 pp3756ndash3764 1996

[32] NOkadaMHamada IOgiwara andKOhshima ldquoSINEs andLINEs share common 31015840 sequences a reviewrdquoGene vol 205 no1-2 pp 229ndash243 1997

[33] A MWeiner ldquoSINEs and LINEs the art of biting the hand thatfeeds yourdquo Current Opinion in Cell Biology vol 14 no 3 pp343ndash350 2002

[34] K Ohshima ldquoParallel relaxation of stringent RNA recognitionin plant and mammalian L1 retrotransposonsrdquo Molecular Biol-ogy and Evolution vol 29 no 11 pp 3255ndash3259 2012

[35] Y Yoshioka S Matsumoto S Kojima K Ohshima N Okadaand Y Machida ldquoMolecular characterization of a short inter-spersed repetitive element from tobacco that exhibits sequencehomology to specific tRNAsrdquo Proceedings of the NationalAcademy of Sciences of the United States of America vol 90 no14 pp 6562ndash6566 1993

[36] M Kajikawa and N Okada ldquoLINEs mobilize SINEs in the eelthrough a shared 31015840 sequencerdquo Cell vol 111 no 3 pp 433ndash4442002

[37] H Takahashi and H Fujiwara ldquoTransplantation of target sitespecificity by swapping the endonuclease domains of twoLINEsrdquoThe EMBO Journal vol 21 no 3 pp 408ndash417 2002

[38] M Osanai H Takahashi K K Kojima M Hamada andH Fujiwara ldquoEssential motifs in the 31015840 untranslated regionrequired for retrotransposition and the precise start of reversetranscription in non-long-terminal-repeat retrotransposonSART1rdquo Molecular and Cellular Biology vol 24 no 18 pp7902ndash7913 2004

[39] T Anzai M Osanai M Hamada and H Fujiwara ldquoFunctionalroles of 31015840-terminal structures of template RNA during in vivoretrotransposition of non-LTR retrotransposon R1BmrdquoNucleicAcids Research vol 33 no 6 pp 1993ndash2002 2005

[40] Q Feng J V Moran H H Kazazian Jr and J D BoekeldquoHuman L1 retrotransposon encodes a conserved endonucleaserequired for retrotranspositionrdquo Cell vol 87 no 5 pp 905ndash9161996

[41] J Jurka ldquoSequence patterns indicate an enzymatic involvementin integration of mammalian retroposonsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 94 no 5 pp 1872ndash1877 1997

[42] A Pavlıcek J Paces D Elleder and J Hejnar ldquoProcessedpseudogenes of human endogenous retroviruses generated byLINEs their integration stability and distributionrdquo GenomeResearch vol 12 no 3 pp 391ndash399 2002

[43] C Esnault J Maestre and T Heidmann ldquoHuman LINE retro-transposons generate processed pseudogenesrdquoNature Geneticsvol 24 no 4 pp 363ndash367 2000

[44] W Wei N Gilbert S L Ooi et al ldquoHuman L1 retrotranspo-sition cis preference versus trans complementationrdquoMolecularand Cellular Biology vol 21 no 4 pp 1429ndash1439 2001

[45] A M Roy-Engel A-H Salem O O Oyeniran et al ldquoActiveAlu element ldquoA-tailsrdquo size does matterrdquo Genome Research vol12 no 9 pp 1333ndash1344 2002

[46] M Dewannieux C Esnault and T Heidmann ldquoLINE-mediated retrotransposition of marked Alu sequencesrdquo NatureGenetics vol 35 no 1 pp 41ndash48 2003


[47] E N Kroutter V P Belancio B J Wagstaff and A M Roy-Engel ldquoThe RNA polymerase dictates ORF1 requirement andtiming of LINE and SINE retrotranspositionrdquo PLoS Geneticsvol 5 no 4 Article ID e1000458 2009

[48] J V Moran S E Holmes T P Naas R J DeBerardinis J DBoeke and H H Kazazian Jr ldquoHigh frequency retrotransposi-tion in cultured mammalian cellsrdquo Cell vol 87 no 5 pp 917ndash927 1996

[49] J V Moran R J DeBerardinis and H H Kazazian Jr ldquoExonshuffling by L1 retrotranspositionrdquo Science vol 283 no 5407pp 1530ndash1534 1999

[50] K Ohshima M Hattori T Yada T Gojobori Y Sakaki and NOkada ldquoWhole-genome screening indicates a possible burst offormation of processed pseudogenes and Alu repeats by partic-ular L1 subfamilies in ancestral primatesrdquo Genome Biology vol4 no 11 article R74 2003

[51] J D Boeke ldquoLINEs and Alusmdashthe polyA connectionrdquo Naturegenetics vol 16 no 1 pp 6ndash7 1997

[52] J Schmitz G Churakov H Zischler and J Brosius ldquoAnovel class of mammalian-specific tailless retropseudogenesrdquoGenome Research vol 14 no 10a pp 1911ndash1915 2004

[53] Z Zhang P M Harrison Y Liu and M Gerstein ldquoMillionsof years of evolution preserved a comprehensive catalog ofthe processed pseudogenes in the human genomerdquo GenomeResearch vol 13 no 12 pp 2541ndash2558 2003

[54] A C Marques I Dupanloup N Vinckenbosch A Reymondand H Kaessmann ldquoEmergence of young human genes after aburst of retroposition in primatesrdquo PLoS Biology vol 3 no 11article e357 2005

[55] H Sakai K O Koyanagi T Imanishi T Itoh and T GojoborildquoFrequent emergence and functional resurrection of processedpseudogenes in the human andmouse genomesrdquoGene vol 389no 2 pp 196ndash203 2007

[56] B J Wagstaff E N Kroutter R S Derbes V P Belancio andA M Roy-Engel ldquoMolecular reconstruction of extinct LINE-1elements and their interaction with nonautonomous elementsrdquoMolecular Biology and Evolution vol 30 no 1 pp 88ndash99 2013

[57] F Burki and H Kaessmann ldquoBirth and adaptive evolution ofa hominoid gene that supports high neurotransmitter fluxrdquoNature Genetics vol 36 no 10 pp 1061ndash1063 2004

[58] L Rosso A C Marques M Weier et al ldquoBirth and rapidsubcellular adaptation of a hominoid-specific CDC14 proteinrdquoPLoS Biology vol 6 no 6 article e140 2008

[59] D V Babushok K Ohshima E M Ostertag et al ldquoA noveltestis ubiquitin-binding protein gene arose by exon shuffling inhominoidsrdquoGenome Research vol 17 no 8 pp 1129ndash1138 2007

[60] Y Zhang S Lu S Zhao X Zheng M Long and L WeildquoPositive selection for themale functionality of a co-retroposedgene in the hominoidsrdquoBMCEvolutionary Biology vol 9 article252 2009

[61] K Ohshima and K Igarashi ldquoInference for the initial stage ofdomain shuffling tracing the evolutionary fate of the PIPSLretrogene in hominoidsrdquo Molecular Biology and Evolution vol27 no 11 pp 2522ndash2533 2010

[62] P M Harrison D Zheng Z Zhang N Carriero and MGerstein ldquoTranscribed processed pseudogenes in the humangenome an intermediate form of expressed retrosequencelacking protein-coding abilityrdquo Nucleic Acids Research vol 33no 8 pp 2374ndash2383 2005

[63] N Vinckenbosch I Dupanloup and H Kaessmann ldquoEvolu-tionary fate of retroposed gene copies in the human genomerdquo

Proceedings of the National Academy of Sciences of the UnitedStates of America vol 103 no 9 pp 3220ndash3225 2006

[64] R Baertsch M Diekhans W J Kent D Haussler and J Bro-sius ldquoRetrocopy contributions to the evolution of the humangenomerdquo BMC Genomics vol 9 article 466 2008

[65] K K Kojima andNOkada ldquomRNA retrotransposition coupledwith 51015840 inversion as a possible source of new genesrdquo MolecularBiology and Evolution vol 26 no 6 pp 1405ndash1420 2009

[66] R S Baucom J C Estill C Chaparro et al ldquoExceptionaldiversity non-random distribution and rapid evolution ofretroelements in the B73 maize genomerdquo PLoS Genetics vol 5no 11 Article ID e1000732 2009

[67] K NomaHOhtsubo and E Ohtsubo ldquoATLN elements LINEsfrom Arabidopsis thaliana identification and characterizationrdquoDNA Research vol 7 no 5 pp 291ndash303 2000

[68] A Lenoir L Lavie J-L Prieto et al ldquoThe evolutionary originand genomic organization of SINEs in Arabidopsis thalianardquoMolecular Biology and Evolution vol 18 no 12 pp 2315ndash23222001

[69] F Myouga S Tsuchimoto K Noma H Ohtsubo and E Oht-subo ldquoIdentification and structural analysis of SINE elementsin theArabidopsis thaliana genomerdquoGenes andGenetic Systemsvol 76 no 3 pp 169ndash179 2001

[70] J Faris A Sirikhachornkit R Haselkorn B Gill and PGornicki ldquoChromosome mapping and phylogenetic analysis ofthe cytosolic acetyl-CoA carboxylase loci in wheatrdquo MolecularBiology and Evolution vol 18 no 9 pp 1720ndash1733 2001

[71] Y Zhang Y Wu Y Liu and B Han ldquoComputational identifi-cation of 69 retroposons in Arabidopsisrdquo Plant Physiology vol138 no 2 pp 935ndash948 2005

[72] D Benovoy and G Drouin ldquoProcessed pseudogenes processedgenes and spontaneous mutations in the Arabidopsis genomerdquoJournal of Molecular Evolution vol 62 no 5 pp 511ndash522 2006

[73] N Nurhayati D Gonde and D Ober ldquoEvolution of pyrrolizi-dine alkaloids in Phalaenopsis orchids and other monocotyle-dons identification of deoxyhypusine synthase homospermi-dine synthase and related pseudogenesrdquoPhytochemistry vol 70no 4 pp 508ndash516 2009

[74] K Mochizuki M Umeda H Ohtsubo and E Ohtsubo ldquoChar-acterization of a plant SINE p-SINE1 in rice genomesrdquo JapaneseJournal of Genetics vol 67 no 2 pp 155ndash166 1992

[75] J-H Xu I Osawa S Tsuchimoto E Ohtsubo and H OhtsuboldquoTwo new SINE elements p-SINE2 and p-SINE3 from ricerdquoGenes and Genetic Systems vol 80 no 3 pp 161ndash171 2005

[76] Y Yasui S Nasuda Y Matsuoka and T Kawahara ldquoThe Aufamily a novel short interspersed element (SINE) fromAegilopsumbellulatardquo Theoretical and Applied Genetics vol 102 no 4pp 463ndash470 2001

[77] J A Fawcett T Kawahara H Watanabe and Y Yasui ldquoASINE family widely distributed in the plant kingdom and itsevolutionary historyrdquo Plant Molecular Biology vol 61 no 3 pp505ndash514 2006

[78] E Yagi T Akita and T Kawahara ldquoA novel Au SINE sequencefound in a gymnospermrdquo Genes and Genetic Systems vol 86no 1 pp 19ndash25 2011

[79] Y Shu Y Li X Bai et al ldquoIdentification and characterization ofa new member of the SINE Au retroposon family (GmAu1) inthe soybean Glycine max (L) Merr genome and its potentialapplicationrdquo Plant Cell Reports vol 30 no 12 pp 2207ndash22132011


[80] M J Moore C D Bell P S Soltis and D E Soltis ldquoUsingplastid genome-scale data to resolve enigmatic relationshipsamong basal angiospermsrdquoProceedings of theNational Academyof Sciences of the United States of America vol 104 no 49 pp19363ndash19368 2007

[81] D H Mathews A R Banerjee D D Luan T H Eickbush andD H Turner ldquoSecondary structure model of the RNA recog-nized by the reverse transcriptase from theR2 retrotransposableelementrdquo RNA vol 3 no 1 pp 1ndash16 1997

[82] Y Nomura M Kajikawa S Baba et al ldquoSolution structure andfunctional importance of a conserved RNA hairpin of eel LINEUnaL2rdquo Nucleic Acids Research vol 34 no 18 pp 5184ndash51932006

[83] V Cognat J-M Deragon E Vinogradova T Salinas CRemacle and L Marechal-Drouard ldquoOn the evolution andexpression of Chlamydomonas reinhardtii nucleus-encodedtransfer RNA genesrdquo Genetics vol 179 no 1 pp 113ndash123 2008

[84] K G Karol R M McCourt M T Cimino and C F DelwicheldquoThe closest living relatives of land plantsrdquo Science vol 294 no5550 pp 2351ndash2353 2001

[85] M G Kidwell and D Lisch ldquoTransposable elements as sourcesof variation in animals and plantsrdquo Proceedings of the NationalAcademy of Sciences of the United States of America vol 94 no15 pp 7704ndash7711 1997

[86] D Kordis and F Gubensek ldquoUnusual horizontal transfer of along interspersed nuclear element between distant vertebrateclassesrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 95 no 18 pp 10704ndash10709 1998

[87] A M Walsh R D Kortschak M G Gardner T Bertozzi andD L Adelson ldquoWidespread horizontal transfer of retrotrans-posonsrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 110 no 3 pp 1012ndash1016 2013

[88] S Chambeyron A Bucheton and I Busseau ldquoTandem UAArepeats at the 31015840-end of the transcript are essential for the preciseinitiation of reverse transcription of the I factor in Drosophilamelanogasterrdquo Journal of Biological Chemistry vol 277 no 20pp 17877ndash17882 2002

[89] M Komatsu K Shimamoto and J Kyozuka ldquoTwo-step regu-lation and continuous retrotransposition of the rice LINE-typeretrotransposonKarmardquo Plant Cell vol 15 no 8 pp 1934ndash19442003

[90] X Zhang and S R Wessler ldquoGenome-wide comparativeanalysis of the transposable elements in the related speciesArabidopsis thaliana and Brassica oleraceardquo Proceedings of theNational Academy of Sciences of the United States of Americavol 101 no 15 pp 5589ndash5594 2004

[91] H Yamashita and M Tahara ldquoA LINE-type retrotransposonactive in meristem stem cells causes heritable transpositions inthe sweet potato genomerdquo Plant Molecular Biology vol 61 no1-2 pp 79ndash94 2006

[92] T Heitkam and T Schmidt ldquoBNRmdasha LINE family from Betavulgarismdashcontains a RRM domain in open reading frame 1 anddefines a L1 sub-clade present in diverse plant genomesrdquo PlantJournal vol 59 no 6 pp 872ndash882 2009

[93] J D Hollister L M Smith Y-L Guo F Ott D Weigel andB S Gaut ldquoTransposable elements and small RNAs contributeto gene expression divergence between Arabidopsis thalianaand Arabidopsis lyratardquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 6 pp 2322ndash2327 2011

[94] E Khazina V Truffault R Buttner S Schmidt M Colesand O Weichenrieder ldquoTrimeric structure and flexibility of

the L1ORF1 protein in human L1 retrotranspositionrdquo NatureStructural and Molecular Biology vol 18 no 9 pp 1006ndash10142011

[95] S J Smerdon J Jager J Wang et al ldquoStructure of the bindingsite for nonnucleoside inhibitors of the reverse transcriptaseof human immunodeficiency virus type 1rdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 91 no 9 pp 3911ndash3915 1994

[96] M Zuker ldquoMfold web server for nucleic acid folding andhybridization predictionrdquoNucleic Acids Research vol 31 no 13pp 3406ndash3415 2003

[97] A F A Smit and A D Riggs ldquoMIRs are classic tRNA-derivedSINEs that amplified before the mammalian radiationrdquo NucleicAcids Research vol 23 no 1 pp 98ndash102 1995

[98] J Jurka E Zietkiewicz and D Labuda ldquoUbiquitousmammalian-wide interspersed repeats (MIRs) are molecularfossils from the mesozoic erardquo Nucleic Acids Research vol 23no 1 pp 170ndash175 1995

[99] N Gilbert and D Labuda ldquoEvolutionary inventions and con-tinuity of CORE-SINEs in mammalsrdquo Journal of MolecularBiology vol 298 no 3 pp 365ndash377 2000

[100] A F A Smit ldquoThe origin of interspersed repeats in the humangenomerdquo Current Opinion in Genetics and Development vol 6no 6 pp 743ndash748 1996

[101] V V Kapitonov and J Jurka ldquoThe esterase and PHD domainsin CR1-like non-LTR retrotransposonsrdquo Molecular Biology andEvolution vol 20 no 1 pp 38ndash46 2003

[102] N Gilbert and D Labuda ldquoCORE-SINEs eukaryotic shortinterspersed retroposing elements with common sequencemotifsrdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 96 no 6 pp 2869ndash2874 1999

[103] K P Gogolevsky N S Vassetzky and D A Kramerov ldquoBov-B-mobilized SINEs in vertebrate genomesrdquo Gene vol 407 no 1-2pp 75ndash85 2008

[104] NOkada andMHamada ldquoThe 31015840 ends of tRNA-derived SINEsoriginated from the 31015840 ends of LINEs a new example fromthe bovine genomerdquo Journal of Molecular Evolution vol 44supplement 1 pp S52ndashS56 1997

[105] J A Lenstra J A van Boxtel K A Zwaagstra andM SchwerinldquoShort interspersed nuclear element (SINE) sequences of theBovidaerdquo Animal Genetics vol 24 no 1 pp 33ndash39 1993

[106] J Szemraj G Płucienniczak J Jaworski and A PłucienniczakldquoBovineAlu-like sequences mediate transposition of a new site-specific retroelementrdquo Gene vol 152 no 2 pp 261ndash264 1995

[107] M Nikaido H Nishihara Y Hukumoto and N OkadaldquoAncient SINEs from African endemic mammalsrdquo MolecularBiology and Evolution vol 20 no 4 pp 522ndash527 2003

[108] C Gilbert J K Pace II and P D Waters ldquoTarget site analysisof RTE1 LA and its AfroSINE partner in the elephant genomerdquoGene vol 425 no 1-2 pp 1ndash8 2008

[109] H Endoh and N Okada ldquoTotal DNA transcription invitro a procedure to detect highly repetitive and transcrib-able sequences with tRNA-like structuresrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 83 no 2 pp 251ndash255 1986

[110] H Endoh S Nagahashi and N Okada ldquoA highly repetitiveand transcribable sequence in the tortoise genome is probablya retroposonrdquo European Journal of Biochemistry vol 189 no 1pp 25ndash31 1990

[111] T Sasaki K Takahashi M Nikaido S Miura Y Yasukawa andN Okada ldquoFirst application of the SINE (Short Interspersed


Repetitive Element) method to infer phylogenetic relationshipsin reptiles an example from the turtle superfamily testudi-noideardquoMolecular Biology and Evolution vol 21 no 4 pp 705ndash715 2004

[112] MKajikawa KOhshima andNOkada ldquoDetermination of theentire sequence of turtle CR1 the first open reading frame of theturtle CR1 element encodes a protein with a novel zinc fingermotifrdquoMolecular Biology and Evolution vol 14 no 12 pp 1206ndash1217 1997

[113] T L Vandergon and M Reitman ldquoEvolution of chicken repeat1 (CR1) elements evidence for ancient subfamilies and multipleprogenitorsrdquoMolecular Biology and Evolution vol 11 no 6 pp886ndash898 1994

[114] O Piskurek C C Austin and N Okada ldquoSauria SINEs novelshort interspersed retroposable elements that are widespread inreptile genomesrdquo Journal of Molecular Evolution vol 62 no 5pp 630ndash644 2006

[115] O Piskurek H Nishihara and N Okada ldquoThe evolution of twopartner LINESINE families and a full-length chromodomain-containing Ty3Gypsy LTR element in the first reptilian genomeof Anolis carolinensisrdquo Gene vol 441 no 1-2 pp 111ndash118 2009

[116] K K Kojima V V Kapitonov and J Jurka ldquoRecent expansionof a new Ingi-related clade of Vingi non-LTR retrotransposonsin hedgehogsrdquo Molecular Biology and Evolution vol 28 no 1pp 17ndash20 2011

[117] K-I Matsumoto K Murakami and N Okada ldquoGene forlysine tRNA

1may be a progenitor of the highly repetitive

and transcribable sequences present in the salmon genomerdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 83 no 10 pp 3156ndash3160 1986

[118] Y Kido M Aono T Yamaki et al ldquoShaping and reshapingof salmonid genomes by amplification of tRNA-derived retro-posons during evolutionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 88 no 6 pp2326ndash2330 1991

[119] V Matveev H Nishihara and N Okada ldquoNovel SINE familiesfrom salmons validate Parahucho (Salmonidae) as a distinctgenus and give evidence that SINEs can incorporate LINE-related 31015840-tails of other SINEsrdquoMolecular Biology and Evolutionvol 24 no 8 pp 1656ndash1666 2007

[120] R J Winkfein R D Moir S A Krawetz J Blanco J C Statesand G H Dixon ldquoA new family of repetitive retroposon-like sequences in the genome of the rainbow troutrdquo EuropeanJournal of Biochemistry vol 176 no 2 pp 255ndash264 1988

[121] Y Terai K Takahashi and N Okada ldquoSINE cousins the 31015840-endtails of the two oldest and distantly related families of SINEs aredescended from the 31015840 ends of LINEswith the same genealogicaloriginrdquoMolecular Biology andEvolution vol 15 no 11 pp 1460ndash1471 1998

[122] K Takahashi Y Terai M Nishida and N Okada ldquoA novelfamily of short interspersed repetitive elements (SINEs) fromcichlids the patterns of insertion of SINEs at orthologousloci support the proposed monophyly of four major groupsof cichlid fishes in Lake Tanganyikardquo Molecular Biology andEvolution vol 15 no 4 pp 391ndash407 1998

[123] MKajikawa K Ichiyanagi N Tanaka andNOkada ldquoIsolationand characterization of active LINE and SINEs from the eelrdquoMolecular Biology and Evolution vol 22 no 3 pp 673ndash6822005

[124] C Tong B Guo and S He ldquoBead-probe complex capture acouple of SINE and LINE family from genomes of two closely

related species of East Asian cyprinid directly using magneticseparationrdquo BMC Genomics vol 10 article 83 2009

[125] H Nishihara A F A Smit andN Okada ldquoFunctional noncod-ing sequences derived from SINEs in the mammalian genomerdquoGenome Research vol 16 no 7 pp 864ndash874 2006

[126] I Ogiwara M Miya K Ohshima and N Okada ldquoRetroposi-tional parasitism of SINEs on LINEs identification of SINEsand LINEs in elasmobranchsrdquoMolecular Biology and Evolutionvol 16 no 9 pp 1238ndash1250 1999

[127] I Ogiwara M Miya K Ohshima and N Okada ldquoV-SINEsa new superfamily of vertebrate SINEs that are widespread invertebrate genomes and retain a strongly conserved segmentwithin each repetitive unitrdquo Genome Research vol 12 no 2 pp316ndash324 2002

[128] Z Izsvak Z Ivics D Garcia-Estefania S C Fahrenkrug andP B Hackett ldquoDANA elements a family of composite tRNA-derived short interspersedDNAelements associatedwithmuta-tional activities in zebrafish (Danio rerio)rdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 93 no 3 pp 1077ndash1081 1996

[129] N Shimoda M Chevrette M Ekker Y Kikuchi Y Hotta andHOkamoto ldquoMermaid a family of short interspersed repetitiveelements is useful for zebrafish genome mappingrdquo Biochemicaland Biophysical Research Communications vol 220 no 1 pp233ndash237 1996

[130] BVenkatesh E F Kirkness Y-H Loh et al ldquoSurvey sequencingand comparative analysis of the elephant shark (Callorhinchusmilii) genomerdquo PLoS Biology vol 5 no 4 article e101 2007

[131] P E Nisson R J Hickey M F Boshar and W R Crain JrldquoIdentification of a repeated sequence in the genome of the seaurchinwhich is traescribed byRNApolymerase III and containsthe features of a retroposonrdquoNucleic Acids Research vol 16 no4 pp 1431ndash1452 1988

[132] Z Tu S Li and C Mao ldquoThe changing tails of a novel shortinterspersed element in Aedes aegypti genomic evidence forslippage retrotransposition and the relationship between 31015840tandem repeats and the poly(dA) tailrdquo Genetics vol 168 no 4pp 2037ndash2047 2004

[133] Z Tu and J J Hill ldquoMosquI a novel family of mosquitoretrotransposons distantly related to the Drosophila I factorsmay consist of elements of more than one originrdquo MolecularBiology and Evolution vol 16 no 12 pp 1675ndash1686 1999

[134] O Piskurek andD J Jackson ldquoTracking the ancestry of a deeplyconserved eumetazoan SINE domainrdquo Molecular Biology andEvolution vol 28 no 10 pp 2727ndash2730 2011

[135] P Kachroo S A Leong and B B Chattoo ldquoMg-SINE ashort interspersed nuclear element from the rice blast fungusMagnaporthe griseardquo Proceedings of the National Academy ofSciences of the United States of America vol 92 no 24 pp 11125ndash11129 1995

[136] A M Shire and J P Ackers ldquoSINE elements of Entamoebadisparrdquo Molecular and Biochemical Parasitology vol 152 no 1pp 47ndash52 2007

[137] K Van Dellen J Field Z Wang B Loftus and J SamuelsonldquoLINEs and SINE-like elements of the protist Entamoebahistolyticardquo Gene vol 297 no 1-2 pp 229ndash239 2002

[138] U Willhoeft H Buszlig and E Tannich ldquoThe abundantpolyadenylated transcript 2 DNA sequence of the pathogenicprotozoan parasite Entamoeba histolytica represents a nonau-tonomous non-long-terminal-repeat retrotransposon-like ele-ment which is absent in the closely related nonpathogenic


species Entamoeba disparrdquo Infection and Immunity vol 70 no12 pp 6798ndash6804 2002

[139] K K Kojima and H Fujiwara ldquoAn extraordinary retrotrans-poson family encoding dual endonucleasesrdquo Genome Researchvol 15 no 8 pp 1106ndash1117 2005

[140] S Tsuchimoto Y Hirao E Ohtsubo and H Ohtsubo ldquoNewSINE families from rice OsSN with poly(A) at the 31015840 endsrdquoGenes and Genetic Systems vol 83 no 3 pp 227ndash236 2008

[141] J-M Deragon B S Landry T Pelissier S Tutois S Tourmenteand G Picard ldquoAn analysis of retroposition in plants based ona family of SINEs from Brassica napusrdquo Journal of MolecularEvolution vol 39 no 4 pp 378ndash386 1994

[142] A Lenoir T Pelissier C Bousquet-Antonelli and J M Der-agon ldquoComparative evolution history of SINEs in Arabidopsisthaliana and Brassica oleracea evidence for a high rate of SINElossrdquo Cytogenetic and Genome Research vol 110 no 1ndash4 pp441ndash447 2005

[143] X Zhang and S R Wessler ldquoBoS a large and diverse familyof short interspersed elements (SINEs) in Brassica oleraceardquoJournal of Molecular Evolution vol 60 no 5 pp 677ndash687 2005

[144] J-M Deragon and X Zhang ldquoShort interspersed elements(SINEs) in plants origin classification and use as phylogeneticmarkersrdquo Systematic Biology vol 55 no 6 pp 949ndash956 2006

[145] M Gadzalski and T Sakowicz ldquoNovel SINEs families in Med-icago truncatula and Lotus japonicus bioinformatic analysisrdquoGene vol 480 no 1-2 pp 21ndash27 2011

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of


Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology


Molecular Biology International

GenomicsInternational Journal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


BioinformaticsAdvances in

Marine BiologyJournal of



Signal TransductionJournal of


BioMed Research International

Evolutionary BiologyInternational Journal of



Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014


Genetics Research International


Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational



Enzyme Research



Microbiology


Gene Processed pseudogene

Transcription

mRNA

SplicingReverse transcriptionand insertion into the genome

Figure 1 Schematic representation of the formation of a processedpseudogene

LINERNA Pol II

ORF1 ORF2

SINEPol III

tRNA or7SLRNA 5SrRNA

ORF1 protein Endonuclease andreverse transcriptase

Figure 2 Schematic representation of a SINE and a LINE that havethe same 31015840-end sequence Three-dimensional protein structuresare taken from the L1-encoded ORF1 protein [94] and the reversetranscriptase of human immunodeficiency virus type 1 [95]

as L1 are also believed to retrotranspose by TPRT [18] Thehuman L1 TPRT machinery has been reconstructed in vitro[19]

SINEs are non-autonomous retroposons the 51015840-endsequences of which are derived from tRNA 5S rRNA or7SL RNA with promoter activity for RNA polymerase III(Figure 2) [20ndash22] On the other hand the 31015840-end sequencesof SINEs generally originated from a corresponding LINE[23] A small nucleolar RNA-derived short retroposon whichlacks internal promoters for RNA polymerase III and hastherefore not been subject to multiple rounds of retroposi-tion was recently discovered in the platypus [24]

13 Evolutionary Relationships of Various LINEs Eickbushrsquosgroup conducted comprehensive phylogenetic analysis ofLINEs using extended sequence alignment of their RTdomains [25] All identified LINEs were grouped into 11distinct clades Assuming vertical descent the phylogenysuggests that LINEs are as old as eukaryotes with eachof the 11 clades dating back approximately 2 billion years[25] Currently almost 30 clades have been recognized [26]Mammalian L1s belong to the L1 clade which includesnumerous LINEs from vertebrates slime mold plants andalgae [25 27 28] Analyses of L1-encoded endonucleases fromzebrafish and mammals revealed that they are divided into3 groups M F and Tx1 [29] Kordis et al showed that thegenomes of deuterostomes possess three highly divergentgroups of L1-clade LINEs which are distinct from Tx group[28] The Tx group with a target-specific insertion consistsof 2 branches one of which includes frog Tx1 [30]

14 SINEs and LINEs The31015840-end sequences of various SINEsoriginated from a corresponding LINE (Figure 2) [31] forreviews see also [23 32 33] A systematic database and liter-ature survey identified 58 SINEs each possessing a common31015840-end sequence with its partner LINE (Table 1) [34] Forexample Figure 3 shows the alignment of tobacco TS SINE[35] with its partner LINE This LINE which was recentlyidentified in the potato genome amember of the same familyas tobacco belongs to the RTE clade The 31015840-end sequenceof the SINE approximately 100 bases is nearly identical tothat of the LINE and they both end in TTG repeats [34]SINELINE pairs have been observed in a wide variety ofspecies from eumetazoans to green plants confirming thegenerality of this phenomenon (Table 1) Although variousLINEs appear in the list those from clades CR1 and RTEwereparticularly predominant

Since the R2 LINE protein specifically recognizes thesequence near the 31015840-end of the RNA transcript for the initi-ation of first-strand synthesis [16 17] the homology betweenthe 31015840-ends of SINEs and LINEs suggests that each SINEfamily recruits the enzymatic machinery for retropositionfrom the corresponding LINE through this common ldquotailrdquosequence [31] This hypothesis was strongly supported byexperiments with SINE sequences in the eel [36] As the 31015840-UTRs of several LINEs have been shown to be essential forretroposition [17 36ndash39] these LINEs presumably requireldquostringentrdquo recognition of the 31015840-end sequence of the RNAtemplate [32 36]

Figure 4 illustrates the relationship between the numberof SINELINE pairs and the number of LINEs in each clade[34] Although Spearmanrsquos rank correlation is not significant(120588 = 025) the number of SINEs with a LINE tail is positivelycorrelated with the number of LINEs belonging to each clade(1198772 = 083) that is more LINEs tend to lead to moreSINELINE pairs Therefore although a few LINE clades arethe predominant source of SINELINE pairs it is plausiblethat this simply reflects the large number of LINEs in theseclades However L1-clade LINEs are the only prominentexception to this Although over 800 L1-clade LINEs appearedin the database only 3 SINEs with L1 tails were found [34]suggesting that in general L1-clade LINEs are different fromother LINEs with regard to 31015840-end recognition

15 Mechanism of RNA-Mediated Gene Duplication in Mam-mals Mammalian PPs and retrogenes were probably mobi-lized by L1s because they end in poly(A) and have L1-typetarget site duplications they are inserted in L1-type endonu-clease cleavage sites [40ndash42] Molecular biological studieshave shown that mammalian L1-encoded proteins have beeninvolved in the reverse transcription of PPs [43 44] In thesame assay another class of autonomous retroposons LTRretrotransposons (retroviral-like elements) were unable toproduce similar PP-like structures [43]

The 31015840-end sequences of mammalian L1 LINEs do notexhibit any similarity to SINEs except for the presence of31015840-poly(A) repeats although these L1s are thought to havemediated the retroposition of mammalian SINEs such as pri-mateAlu and rodent B1 families [45ndash47] Since the 31015840-poly(A)


Box A Box B







TSRTE-1 STu

TSRTE-1 STu

TSRTE-1 STu 4095

207

4051177

396190




0

5

10

15

20

25

30

0 200 400 600 800

SIN

Es

LINEs

CR1L2

RTE

L1a

bc

d ef g

R2 = 08343


























Amphibians


(L2-3 L2-6 L2-2) [15] [15 34]


Fish






Table 1 Continued











tRNA HER1 [126] [126]




Chordates


Deuterostomes



tRNA CR1-4 SP [15] [34]







Protostomes



I-64I Ele10 14 35 37)

[15 133] [34 132]

Eumetazoans






Fungi



(HaTad1-3 1-5) [15] [34]


Table 1 Continued





Land plants



























lowastb 0L1 15 2

lowasta8lowastc 5


RTEX 6 0 6lowaste 0












Human PIPSL

Chimp PIPSL

Gorilla PIPSL

Orang PIPSL

Gibbon PIPSL

Human

Chimpanzee

Orangutan

Macaque

Cow

Dog

Mouse

PIP5K

0 21

005 S5a

30 10

102 73

168 20

71 10

0 00 56

41 4161 061 6251 11

10 0

0 4116 241

10 310 11

10 93

36 548

14 5680 133

137 956


050

100150200250300350400

R4 L1

RTE

CR1

and

L2

Rex1

Crac

k

Ving

i I

Oth

ers


vertebrates








|||||||||||||| || ||| ||||| ||||||| |

| || || ||||| ||| || || | || || | |

| ||||| || |||||| |||||||||||||||




Monocot 1a

LINE1-1 ZM

SINE2 consensus


UCCC

C

C

C

CC

U

UG

GG

G

G

GGG

A

UUUUUU U

AAAAAA

UUA

A


12

C CC

C

CC

C

CC

UU

UG

GG

G

GG

GG

A

UU

U

UUU UU UAAAAAA A

12

UU

C C

C

C

C

G

GCG

G

C

C

GCG

GGGGG

G

UA

U

UU U

A

AA AA A

U

A

LINE1-1 ZM


C

CC

G

GC

CC

CC C C

GG

G

GG G G

G

GG

U

U

UUUUU

U

UU

U

A

AAAAAA A

3

4

CC

C

CC

C

G

G

CC

CC C C

G

GCG

GG G G

G

GG

U

UUUUU

U

UU

U

A

AAAAAA A

C

C CC

CC

CGCGC

C

C

G

G

GCG

G

GG

GGGG

UUU

AAA

CC

C

G

G UUU

CAU

UU UU AA A

U

A

5

SINE2-1 SBi

C

C

GCG

CGC

CC

GG

C GC

CG

GGG UUU AAAA

A

CC

G

C GA

A

5

UU A


C

C C

GCG

CG

CG

CC

G

C

C

G

G

GGG

UG U

U

UUU AA A AUU A

CGG

SINE2-1c SBi

3

4





ME1

ME2

ME3

M

F

MonocotsEudicots

MammalsFishes

Loss

Loss

Stringent

Green algae

MonocotsEudicots

MonocotsEudicots

Fishes









Acknowledgment


References






































































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Box A Box B







TSRTE-1 STu

TSRTE-1 STu

TSRTE-1 STu 4095

207

4051177

396190




0

5

10

15

20

25

30

0 200 400 600 800

SIN

Es

LINEs

CR1L2

RTE

L1a

bc

d ef g

R2 = 08343


























Amphibians


(L2-3 L2-6 L2-2) [15] [15 34]


Fish






Table 1 Continued











tRNA HER1 [126] [126]




Chordates


Deuterostomes



tRNA CR1-4 SP [15] [34]







Protostomes



I-64I Ele10 14 35 37)

[15 133] [34 132]

Eumetazoans






Fungi



(HaTad1-3 1-5) [15] [34]


Table 1 Continued





Land plants



























lowastb 0L1 15 2

lowasta8lowastc 5


RTEX 6 0 6lowaste 0












Human PIPSL

Chimp PIPSL

Gorilla PIPSL

Orang PIPSL

Gibbon PIPSL

Human

Chimpanzee

Orangutan

Macaque

Cow

Dog

Mouse

PIP5K

0 21

005 S5a

30 10

102 73

168 20

71 10

0 00 56

41 4161 061 6251 11

10 0

0 4116 241

10 310 11

10 93

36 548

14 5680 133

137 956


050

100150200250300350400

R4 L1

RTE

CR1

and

L2

Rex1

Crac

k

Ving

i I

Oth

ers


vertebrates








|||||||||||||| || ||| ||||| ||||||| |

| || || ||||| ||| || || | || || | |

| ||||| || |||||| |||||||||||||||




Monocot 1a

LINE1-1 ZM

SINE2 consensus


UCCC

C

C

C

CC

U

UG

GG

G

G

GGG

A

UUUUUU U

AAAAAA

UUA

A


12

C CC

C

CC

C

CC

UU

UG

GG

G

GG

GG

A

UU

U

UUU UU UAAAAAA A

12

UU

C C

C

C

C

G

GCG

G

C

C

GCG

GGGGG

G

UA

U

UU U

A

AA AA A

U

A

LINE1-1 ZM


C

CC

G

GC

CC

CC C C

GG

G

GG G G

G

GG

U

U

UUUUU

U

UU

U

A

AAAAAA A

3

4

CC

C

CC

C

G

G

CC

CC C C

G

GCG

GG G G

G

GG

U

UUUUU

U

UU

U

A

AAAAAA A

C

C CC

CC

CGCGC

C

C

G

G

GCG

G

GG

GGGG

UUU

AAA

CC

C

G

G UUU

CAU

UU UU AA A

U

A

5

SINE2-1 SBi

C

C

GCG

CGC

CC

GG

C GC

CG

GGG UUU AAAA

A

CC

G

C GA

A

5

UU A


C

C C

GCG

CG

CG

CC

G

C

C

G

G

GGG

UG U

U

UUU AA A AUU A

CGG

SINE2-1c SBi

3

4





ME1

ME2

ME3

M

F

MonocotsEudicots

MammalsFishes

Loss

Loss

Stringent

Green algae

MonocotsEudicots

MonocotsEudicots

Fishes









Acknowledgment


References






































































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


















Amphibians


(L2-3 L2-6 L2-2) [15] [15 34]


Fish






Table 1 Continued











tRNA HER1 [126] [126]




Chordates


Deuterostomes



tRNA CR1-4 SP [15] [34]







Protostomes



I-64I Ele10 14 35 37)

[15 133] [34 132]

Eumetazoans






Fungi



(HaTad1-3 1-5) [15] [34]


Table 1 Continued





Land plants



























lowastb 0L1 15 2

lowasta8lowastc 5


RTEX 6 0 6lowaste 0












Human PIPSL

Chimp PIPSL

Gorilla PIPSL

Orang PIPSL

Gibbon PIPSL

Human

Chimpanzee

Orangutan

Macaque

Cow

Dog

Mouse

PIP5K

0 21

005 S5a

30 10

102 73

168 20

71 10

0 00 56

41 4161 061 6251 11

10 0

0 4116 241

10 310 11

10 93

36 548

14 5680 133

137 956


050

100150200250300350400

R4 L1

RTE

CR1

and

L2

Rex1

Crac

k

Ving

i I

Oth

ers


vertebrates








|||||||||||||| || ||| ||||| ||||||| |

| || || ||||| ||| || || | || || | |

| ||||| || |||||| |||||||||||||||




Monocot 1a

LINE1-1 ZM

SINE2 consensus


UCCC

C

C

C

CC

U

UG

GG

G

G

GGG

A

UUUUUU U

AAAAAA

UUA

A


12

C CC

C

CC

C

CC

UU

UG

GG

G

GG

GG

A

UU

U

UUU UU UAAAAAA A

12

UU

C C

C

C

C

G

GCG

G

C

C

GCG

GGGGG

G

UA

U

UU U

A

AA AA A

U

A

LINE1-1 ZM


C

CC

G

GC

CC

CC C C

GG

G

GG G G

G

GG

U

U

UUUUU

U

UU

U

A

AAAAAA A

3

4

CC

C

CC

C

G

G

CC

CC C C

G

GCG

GG G G

G

GG

U

UUUUU

U

UU

U

A

AAAAAA A

C

C CC

CC

CGCGC

C

C

G

G

GCG

G

GG

GGGG

UUU

AAA

CC

C

G

G UUU

CAU

UU UU AA A

U

A

5

SINE2-1 SBi

C

C

GCG

CGC

CC

GG

C GC

CG

GGG UUU AAAA

A

CC

G

C GA

A

5

UU A


C

C C

GCG

CG

CG

CC

G

C

C

G

G

GGG

UG U

U

UUU AA A AUU A

CGG

SINE2-1c SBi

3

4





ME1

ME2

ME3

M

F

MonocotsEudicots

MammalsFishes

Loss

Loss

Stringent

Green algae

MonocotsEudicots

MonocotsEudicots

Fishes









Acknowledgment


References






































































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Table 1 Continued











tRNA HER1 [126] [126]




Chordates


Deuterostomes



tRNA CR1-4 SP [15] [34]







Protostomes



I-64I Ele10 14 35 37)

[15 133] [34 132]

Eumetazoans






Fungi



(HaTad1-3 1-5) [15] [34]


Table 1 Continued





Land plants



























lowastb 0L1 15 2

lowasta8lowastc 5


RTEX 6 0 6lowaste 0












Human PIPSL

Chimp PIPSL

Gorilla PIPSL

Orang PIPSL

Gibbon PIPSL

Human

Chimpanzee

Orangutan

Macaque

Cow

Dog

Mouse

PIP5K

0 21

005 S5a

30 10

102 73

168 20

71 10

0 00 56

41 4161 061 6251 11

10 0

0 4116 241

10 310 11

10 93

36 548

14 5680 133

137 956


050

100150200250300350400

R4 L1

RTE

CR1

and

L2

Rex1

Crac

k

Ving

i I

Oth

ers


vertebrates








|||||||||||||| || ||| ||||| ||||||| |

| || || ||||| ||| || || | || || | |

| ||||| || |||||| |||||||||||||||




Monocot 1a

LINE1-1 ZM

SINE2 consensus


UCCC

C

C

C

CC

U

UG

GG

G

G

GGG

A

UUUUUU U

AAAAAA

UUA

A


12

C CC

C

CC

C

CC

UU

UG

GG

G

GG

GG

A

UU

U

UUU UU UAAAAAA A

12

UU

C C

C

C

C

G

GCG

G

C

C

GCG

GGGGG

G

UA

U

UU U

A

AA AA A

U

A

LINE1-1 ZM


C

CC

G

GC

CC

CC C C

GG

G

GG G G

G

GG

U

U

UUUUU

U

UU

U

A

AAAAAA A

3

4

CC

C

CC

C

G

G

CC

CC C C

G

GCG

GG G G

G

GG

U

UUUUU

U

UU

U

A

AAAAAA A

C

C CC

CC

CGCGC

C

C

G

G

GCG

G

GG

GGGG

UUU

AAA

CC

C

G

G UUU

CAU

UU UU AA A

U

A

5

SINE2-1 SBi

C

C

GCG

CGC

CC

GG

C GC

CG

GGG UUU AAAA

A

CC

G

C GA

A

5

UU A


C

C C

GCG

CG

CG

CC

G

C

C

G

G

GGG

UG U

U

UUU AA A AUU A

CGG

SINE2-1c SBi

3

4





ME1

ME2

ME3

M

F

MonocotsEudicots

MammalsFishes

Loss

Loss

Stringent

Green algae

MonocotsEudicots

MonocotsEudicots

Fishes









Acknowledgment


References






































































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Table 1 Continued





Land plants



























lowastb 0L1 15 2

lowasta8lowastc 5


RTEX 6 0 6lowaste 0












Human PIPSL

Chimp PIPSL

Gorilla PIPSL

Orang PIPSL

Gibbon PIPSL

Human

Chimpanzee

Orangutan

Macaque

Cow

Dog

Mouse

PIP5K

0 21

005 S5a

30 10

102 73

168 20

71 10

0 00 56

41 4161 061 6251 11

10 0

0 4116 241

10 310 11

10 93

36 548

14 5680 133

137 956


050

100150200250300350400

R4 L1

RTE

CR1

and

L2

Rex1

Crac

k

Ving

i I

Oth

ers


vertebrates








|||||||||||||| || ||| ||||| ||||||| |

| || || ||||| ||| || || | || || | |

| ||||| || |||||| |||||||||||||||




Monocot 1a

LINE1-1 ZM

SINE2 consensus


UCCC

C

C

C

CC

U

UG

GG

G

G

GGG

A

UUUUUU U

AAAAAA

UUA

A


12

C CC

C

CC

C

CC

UU

UG

GG

G

GG

GG

A

UU

U

UUU UU UAAAAAA A

12

UU

C C

C

C

C

G

GCG

G

C

C

GCG

GGGGG

G

UA

U

UU U

A

AA AA A

U

A

LINE1-1 ZM


C

CC

G

GC

CC

CC C C

GG

G

GG G G

G

GG

U

U

UUUUU

U

UU

U

A

AAAAAA A

3

4

CC

C

CC

C

G

G

CC

CC C C

G

GCG

GG G G

G

GG

U

UUUUU

U

UU

U

A

AAAAAA A

C

C CC

CC

CGCGC

C

C

G

G

GCG

G

GG

GGGG

UUU

AAA

CC

C

G

G UUU

CAU

UU UU AA A

U

A

5

SINE2-1 SBi

C

C

GCG

CGC

CC

GG

C GC

CG

GGG UUU AAAA

A

CC

G

C GA

A

5

UU A


C

C C

GCG

CG

CG

CC

G

C

C

G

G

GGG

UG U

U

UUU AA A AUU A

CGG

SINE2-1c SBi

3

4





ME1

ME2

ME3

M

F

MonocotsEudicots

MammalsFishes

Loss

Loss

Stringent

Green algae

MonocotsEudicots

MonocotsEudicots

Fishes









Acknowledgment


References






































































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology
















lowastb 0L1 15 2

lowasta8lowastc 5


RTEX 6 0 6lowaste 0












Human PIPSL

Chimp PIPSL

Gorilla PIPSL

Orang PIPSL

Gibbon PIPSL

Human

Chimpanzee

Orangutan

Macaque

Cow

Dog

Mouse

PIP5K

0 21

005 S5a

30 10

102 73

168 20

71 10

0 00 56

41 4161 061 6251 11

10 0

0 4116 241

10 310 11

10 93

36 548

14 5680 133

137 956


050

100150200250300350400

R4 L1

RTE

CR1

and

L2

Rex1

Crac

k

Ving

i I

Oth

ers


vertebrates








|||||||||||||| || ||| ||||| ||||||| |

| || || ||||| ||| || || | || || | |

| ||||| || |||||| |||||||||||||||




Monocot 1a

LINE1-1 ZM

SINE2 consensus


UCCC

C

C

C

CC

U

UG

GG

G

G

GGG

A

UUUUUU U

AAAAAA

UUA

A


12

C CC

C

CC

C

CC

UU

UG

GG

G

GG

GG

A

UU

U

UUU UU UAAAAAA A

12

UU

C C

C

C

C

G

GCG

G

C

C

GCG

GGGGG

G

UA

U

UU U

A

AA AA A

U

A

LINE1-1 ZM


C

CC

G

GC

CC

CC C C

GG

G

GG G G

G

GG

U

U

UUUUU

U

UU

U

A

AAAAAA A

3

4

CC

C

CC

C

G

G

CC

CC C C

G

GCG

GG G G

G

GG

U

UUUUU

U

UU

U

A

AAAAAA A

C

C CC

CC

CGCGC

C

C

G

G

GCG

G

GG

GGGG

UUU

AAA

CC

C

G

G UUU

CAU

UU UU AA A

U

A

5

SINE2-1 SBi

C

C

GCG

CGC

CC

GG

C GC

CG

GGG UUU AAAA

A

CC

G

C GA

A

5

UU A


C

C C

GCG

CG

CG

CC

G

C

C

G

G

GGG

UG U

U

UUU AA A AUU A

CGG

SINE2-1c SBi

3

4





ME1

ME2

ME3

M

F

MonocotsEudicots

MammalsFishes

Loss

Loss

Stringent

Green algae

MonocotsEudicots

MonocotsEudicots

Fishes









Acknowledgment


References






































































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Human PIPSL

Chimp PIPSL

Gorilla PIPSL

Orang PIPSL

Gibbon PIPSL

Human

Chimpanzee

Orangutan

Macaque

Cow

Dog

Mouse

PIP5K

0 21

005 S5a

30 10

102 73

168 20

71 10

0 00 56

41 4161 061 6251 11

10 0

0 4116 241

10 310 11

10 93

36 548

14 5680 133

137 956


050

100150200250300350400

R4 L1

RTE

CR1

and

L2

Rex1

Crac

k

Ving

i I

Oth

ers


vertebrates








|||||||||||||| || ||| ||||| ||||||| |

| || || ||||| ||| || || | || || | |

| ||||| || |||||| |||||||||||||||




Monocot 1a

LINE1-1 ZM

SINE2 consensus


UCCC

C

C

C

CC

U

UG

GG

G

G

GGG

A

UUUUUU U

AAAAAA

UUA

A


12

C CC

C

CC

C

CC

UU

UG

GG

G

GG

GG

A

UU

U

UUU UU UAAAAAA A

12

UU

C C

C

C

C

G

GCG

G

C

C

GCG

GGGGG

G

UA

U

UU U

A

AA AA A

U

A

LINE1-1 ZM


C

CC

G

GC

CC

CC C C

GG

G

GG G G

G

GG

U

U

UUUUU

U

UU

U

A

AAAAAA A

3

4

CC

C

CC

C

G

G

CC

CC C C

G

GCG

GG G G

G

GG

U

UUUUU

U

UU

U

A

AAAAAA A

C

C CC

CC

CGCGC

C

C

G

G

GCG

G

GG

GGGG

UUU

AAA

CC

C

G

G UUU

CAU

UU UU AA A

U

A

5

SINE2-1 SBi

C

C

GCG

CGC

CC

GG

C GC

CG

GGG UUU AAAA

A

CC

G

C GA

A

5

UU A


C

C C

GCG

CG

CG

CC

G

C

C

G

G

GGG

UG U

U

UUU AA A AUU A

CGG

SINE2-1c SBi

3

4





ME1

ME2

ME3

M

F

MonocotsEudicots

MammalsFishes

Loss

Loss

Stringent

Green algae

MonocotsEudicots

MonocotsEudicots

Fishes









Acknowledgment


References






































































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


|||||||||||||| || ||| ||||| ||||||| |

| || || ||||| ||| || || | || || | |

| ||||| || |||||| |||||||||||||||




Monocot 1a

LINE1-1 ZM

SINE2 consensus


UCCC

C

C

C

CC

U

UG

GG

G

G

GGG

A

UUUUUU U

AAAAAA

UUA

A


12

C CC

C

CC

C

CC

UU

UG

GG

G

GG

GG

A

UU

U

UUU UU UAAAAAA A

12

UU

C C

C

C

C

G

GCG

G

C

C

GCG

GGGGG

G

UA

U

UU U

A

AA AA A

U

A

LINE1-1 ZM


C

CC

G

GC

CC

CC C C

GG

G

GG G G

G

GG

U

U

UUUUU

U

UU

U

A

AAAAAA A

3

4

CC

C

CC

C

G

G

CC

CC C C

G

GCG

GG G G

G

GG

U

UUUUU

U

UU

U

A

AAAAAA A

C

C CC

CC

CGCGC

C

C

G

G

GCG

G

GG

GGGG

UUU

AAA

CC

C

G

G UUU

CAU

UU UU AA A

U

A

5

SINE2-1 SBi

C

C

GCG

CGC

CC

GG

C GC

CG

GGG UUU AAAA

A

CC

G

C GA

A

5

UU A


C

C C

GCG

CG

CG

CC

G

C

C

G

G

GGG

UG U

U

UUU AA A AUU A

CGG

SINE2-1c SBi

3

4





ME1

ME2

ME3

M

F

MonocotsEudicots

MammalsFishes

Loss

Loss

Stringent

Green algae

MonocotsEudicots

MonocotsEudicots

Fishes









Acknowledgment


References






































































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


ME1

ME2

ME3

M

F

MonocotsEudicots

MammalsFishes

Loss

Loss

Stringent

Green algae

MonocotsEudicots

MonocotsEudicots

Fishes









Acknowledgment


References






































































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


























































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

review article rna-mediated gene duplication and...

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