Chromosomal distribution of the retroelements Rex 1, Rex 3 and Rex 6 in species of the genus Harttia and Hypostomus (Siluriformes: Loricariidae)

ABSTRACT

The transposable elements (TE) have been widely applied as physical chromosome markers. However, in Loricariidae there are few physical mapping analyses of these elements. Considering the importance of transposable elements for chromosomal evolution and genome organization, this study conducted the physical chromosome mapping of retroelements (RTEs) Rex1, Rex3 and Rex6 in seven species of the genus Harttia and four species of the genus Hypostomus, aiming to better understand the organization and dynamics of genomes of Loricariidae species. The results showed an intense accumulation of RTEs Rex1, Rex3 and Rex6 and dispersed distribution in heterochromatic and euchromatic regions in the genomes of the species studied here. The presence of retroelements in some chromosomal regions suggests their participation in various chromosomal rearrangements. In addition, the intense accumulation of three retroelements in all species of Harttia and Hypostomus, especially in euchromatic regions, can indicate the participation of these elements in the diversification and evolution of these species through the molecular domestication by genomes of hosts, with these sequences being a co-option for new functions.

Keywords:
Armored catfish; Fluorescence in situ hybridization; Hypostominae; Loricariinae; Transposable elements

RESUMO

Os elementos transponíveis (TE) têm sido amplamente aplicados como marcadores cromossômicos. Contudo, em Loricariidae, há poucas análises de mapeamento físico destes elementos. Considerando a importância de elementos transponíveis para a evolução cromossômica e organização genômica, este trabalho realizou o mapeamento físico cromossômico dos retroelementos (RTEs) Rex1, Rex3 e Rex6 em sete espécies do gênero Harttia e em quatro espécies do gênero Hypostomus, com o intuito de melhor compreender a organização e dinâmica dos genomas das espécies de Loricariidae. Os resultados evidenciaram um intenso acúmulo dos RTEs Rex1, Rex3 e Rex6 e distribuição dispersa em regiões heterocromáticas e eucromáticas no genoma das espécies estudadas. A presença de retroelementos em algumas regiões cromossômicas sugere sua participação em vários rearranjos cromossômicos. Além disso, o intenso acúmulo dos três retroelementos em todas as espécies de Harttia e Hypostomus, especialmente em regiões eucromáticas, pode indicar a participação destes elementos na diversificação e evolução destas espécies através da domesticação molecular pelo genoma dos hospedeiros, com estas sequências sendo co-optadas paras novas funções.

Palavras-chave:
Cascudos; Elementos transponíveis; Hibridização in situ fluorescente; Hypostominae; Loricariinae

Introduction

Repetitive elements have been widely applied as physical chromosome markers in comparative studies for localization of chromosomal rearrangements, identification and characterization of sex chromosomes, and chromosomal evolution analysis (Ferreira et al., 2011a). Among the various sequences used, the transposable elements (TEs) have been gaining space in studies on molecular cytogenetics.

The TEs represent a significant portion of the genome of eukaryotes, being their main feature the mobility within the genome (Hartl et al., 1992). The insertion capacity of the TEs in different locations of the genome can change the function of the genes associated with them (Capy et al., 1998). This dynamic character causes TEs to have a major influence on the composition and evolution of the genome of animals and plants. According to their mechanism of transposition, the TEs are classified as retrotransposons (Class I - transposition occur via an RNA intermediate) or DNA transposons (Class II - transposition occur via DNA) (Biscotti et al., 2015; Carducci et al., 2018).

The class of retrotransposons includes long terminal repeat (LTR) retrotransposons and non-LTR retrotransposons (Biscotti et al., 2015; Carducci et al., 2018). According to Volff et al. (1999, 2001, 2002), the retroelements Rex1, Rex3 and Rex6 are abundant in the teleost genomes. This way, they have been the object of several studies on fish (Fischer et al., 2004; Teixeira et al., 2009; Schneider et al., 2013).

Despite Rex1, Rex3 and Rex6 are usually analyzed together, they have differences in structural organization (Carducci et al., 2018). Rex1 comprises apurinic/apyrimidinic endonuclease sequences located upstream (or downstream) of the reverse transcriptase domain, a conserved 3’-untranslated region followed by an oligonucleotide sequence (Volff et al., 2000; Carducci et al., 2018). Rex3 is characterized by domains of reverse transcriptase, absence of LTR flanking regions, a 3’-end that comprises two repeats of GAA and tandem repeats of GATC, and the stop codon that are located at 3 nucleotides upstream of the first GAA repeat. Rex6 consists of a reverse transcriptase and a putative restriction enzyme-like endonuclease (Carducci et al., 2018).

Loricariidae is composed of 983 valid species (Fricke et al., 2019). Within this family, Hypostominae and Loricariinae are among the subfamilies with the highest number of species and chromosomal diversity. Harttia is a genus of the subfamily Loricariinae that has 26 valid species (Fricke et al., 2019). Of these, only eight species present cytogenetic data (Alves et al., 2003; Kavalco et al., 2005; Centofante et al., 2006; Rodrigues, 2010; Blanco et al., 2012a, 2013, 2014, 2017). The genus Harttia has conspicuous karyotype diversity, with diploid numbers (2n) ranging from 52 chromosomes in Harttia carvalhoi Miranda Ribeiro, 1939 females (Centofante et al., 2006) to 62 chromosomes in Harttia absaberi Oyakawa, Fichberg & Langeani, 2013 (cited as Harttia sp. n) (Rodrigues, 2010). The genus Hypostomus belongs to the subfamily Hypostominae. More than 120 species are described for this genus (Zawadzki et al., 2010), of which only a small number presents cytogenetic studies (Bitencourt et al., 2012; Traldi et al., 2012, 2013a, 2013b). This genus is little conserved from the chromosomal standpoint, with 2n ranging from 54 chromosomes for Hypostomus plecostomus (Linnaeus, 1758) (Muramoto et al., 1968) to 84 chromosomes for Hypostomus sp. 2 (Cereali et al., 2008).

This study conducted the chromosome mapping of retroelements Rex1, Rex3 and Rex6 in species of the genus Harttia and Hypostomus, aiming to better understand the organization of the genomes and chromosomal evolution of species of the Loricariidae family.

Material and Methods

Species analyzed and chromosome preparations. Seven species of the genus Harttia and four species of the genus Hypostomus from different Brazilian river basins were analyzed (Tab. 1). The procedures were performed according to the Ethics Committee on Animal Experimentation (process: 13/2014) of the Universidade Estadual de Ponta Grossa (UEPG), Brazil. The animals were identified and deposited at the Museu de Zoologia da Universidade de São Paulo (MZUSP), Brazil (Tab. 1). The metaphase chromosomes were obtained from portions of the anterior kidney, following the protocols described (Foresti et al., 1993; Blanco et al., 2012b).

Tab. 1
Information of the species collected.

Species	Locality	Hidrographic Basin	GPS	Voucher numbers	Specimens analyzed
Harttia
H. gracilis	Machadinho Stream, Santo Antônio do Pinhal - SP, Brazil	Sapucaí-Mirin	S: 22º48’31” W: 45º41’21”	MZUSP 111384	7 ♂ 6 ♀
H. carvalhoi	Grande Stream, Pindamonhangaba - SP, Brazil	Paraíba do Sul	S: 22º47’08” W: 45º 27’19”	MZUSP 109782	8 ♂ 6 ♀
H. kronei	Açungui River, Campo Largo - PR, Brazil	Ribeira	S: 25º22’44” W: 49º39’08”	MZUSP 109783	8 ♂ 9 ♀
H. longipinna	São Francisco River, Pirapora - MG, Brazil	São Francisco	S: 17º21’22,8” W: 44º56’59,5”	MZUSP 106767	5 ♂ 7 ♀
H. loricariformis	Paraitinga River, Cunha - SP, Brazil	Paraíba do Sul	S: 22º52’22” W: 44º51’0,2”	MZUSP 111386	6 ♂ 8 ♀
H. punctata	Itiquira River, Formosa - GO, Brazil	Tocantins	S: 15º19’25” W: 47º25 26”	MZUSP 111385	8 ♂ 10 ♀
H. torrenticola	Araras Stream, Doresópolis - MG, Brazil	São Francisco	S: 20º16’15” W: 45º55’39”	MZUSP 109784	6 ♂ 7 ♀
Hypostomus
H. ancistroides	Lapa Stream, Ipeúna - SP, Brazil	Corumbataí	S: 22º23’10,1” W: 47º47’0,01”	MZUSP 110802	10 ♂ 8 ♀
H. iheringii	Lapa Stream, Ipeúna - SP, Brazil	Corumbataí	S: 22º23’10,1” W: 47º47’0,01”	MZUSP 106769	5 ♂ 6 ♀
H. nigromaculatus	Lapa Stream, Ipeúna - SP, Brazil	Corumbataí	S: 22º23’10,1” W: 47º47’0,01”	MZUSP 110801	7 ♂ 5 ♀
H. tapijara	Ribeira de Iguape River, Registro - SP, Brazil	Ribeira	S: 24º29’25,35” W: 9º49’4910”	MZUSP 109785	9 ♂ 10 ♀

DNA extraction and isolation of retroelement. Genomic DNA extraction was performed using 0,05g of liver from a sample of Harttia kronei Miranda Ribeiro, 1908 and Hypostomus nigromaculatus (Schubart, 1964), stored in absolute alcohol, according to the phenol-chloroform method (Sambrook et al., 2001). Retroelements Rex1, Rex3 and Rex6 were amplified by PCR using the primers described (Volff et al., 1999, 2000, 2001). The reactions were carried out for a final volume of 25 µl, containing 100-200 ng of genomic DNA, 0.2 µM of each primer, 0.16 mM of dNTPs, 0.5 U of Taq DNA polymerase (Invitrogen^®), 1.5 mM of magnesium chloride, 10x Buffer (without chloride), and distilled water. PCR cycle conditions were: 95°C for 5 minutes, 35 cycles at 95°C for 40 seconds, 55°C for 40 seconds and 72°C for 2 minutes, with subsequent final extension cycle at 72°C for 5 minutes. The amplified fragments were analyzed in agarose gel 1%, measured in spectrophotometry device (BioPhotometer - Eppendorf). PCR reactions with the same conditions described above were performed with Biotin-11-dUTP (Roche Applied Science) for use of these products as probes for fluorescence in situ hybridization (FISH).

Sequencing and analysis of sequences. PCR products were purified using the GFX PCR DNA and Gel Purification kit of Amersham-Pharmacia Biotech. Sequencing reactions were carried out using the DYEnamic ET Dye Terminator kit (with Thermo Sequenase™ II DNA polymerase) according to the protocol for the MegaBACE 1000. The edition of sequences Rex1, Rex3 and Rex6 of H. kronei and H. nigromaculatus was performed with the software BioEdit Sequence Alignment Editor, version 7.0.5.3 (Hall et al., 1999). Subsequently, these sequences were deposited in the GenBank database (http://www.ncbi.nih.gov).

Fluorescence in situ hybridization. All hybridization processes followed the protocol described (Pinkel et al., 1986), about high stringency condition of 77% (200 ng of each probe, 50% formamide, 10% dextran sulfate, 2xSSC, pH 7.0 - 7.2, at 37^oC overnight). After hybridization, the slides were washed twice in 15% formamide/0.2xSSC at 42°C for 10 minutes each, and then two washes of five minutes each were performed in 4xSSC/0.05% Tween at room temperature. The metaphases were analyzed in an epifluorescence microscope (Olympus BX51), and the images were captured by the camera system (Olympus DP72).

Results

Isolation of elements Rex1, Rex3 and Rex6. The partial sequences of retrotransposons Rex1, Rex3 and Rex6 isolated from H. kronei and H. nigromaculatus presented between 430 and 555 base pairs and were deposited in the GenBank database (Tab. 2).

Tab. 2
Retroelements obtained in the present work.

Species	Retroelements	Size	GenBank number	Similarity values with sequences of GenBank
Harttia kronei	Rex1	548pb	MH595484	66.73% - Otocinclus flexilis Cope, 1894 (GQ505951.1)
Hypostomus nigromaculatus	Rex1	553pb	MH595485	83.81% - Hisonotus leucofrenatus (Miranda Ribeiro, 1908) (GQ505952.1) 72.64% - Pseudotocinclus tietensis (Ihering, 1907) (GQ505953.1)
Harttia kronei	Rex3	433pb	MH595486	91.63% - Characidium gomesi Travassos, 1956 (MG028000.1) 89.65% - Pseudotocinclus tietensis (GQ505954.1)
Hypostomus nigromaculatus	Rex3	436pb	MH595487	91.41% - Characidium gomesi (MG028000.1) 90.38% - Pseudotocinclus tietensis (GQ505954.1)
Harttia kronei	Rex6	535pb	MH595488	76.45% - Cichla kelberi Kullander & Ferreira, 2006 (FJ687589.1)
Hypostomus nigromaculatus	Rex6	549pb	MH595480	82.60% - Cichla kelberi (FJ687589.1) 81.28% - Astronotus ocellatus (Agassiz, 1831) (HM535309.1)

Physical mapping of the elements Rex1, Rex3 and Rex6 by FISH. In all species analyzed in this study, the elements Rex1, Rex3 and Rex6 were present in most chromosomes, both in euchromatic and heterochromatic regions, occurring variations in quantities of the three retroelements in the species (Figs. 1, 2 and 3).

In Harttia longipinna Langeani, Oyakawa, Montoya-Burgos, 2001, it is notable the absence of hybridization signal of Rex elements in a conspicuous heterochromatic block of the pair 23 and in supernumerary chromosomes (Fig. 1). In Harttia torrenticola Oyakawa, 1993, Rex elements were not found in the prominent block located in the centromeric heterochromatin of the largest metacentric pair (pair 1) and in the allocated block in terminal position of the long arm of the largest acrocentric pair (pair 22) (Fig. 2). In H. carvalhoi, it is notable that in the first metacentric pair (X chromosome), in contrast to that found in H. torrenticola, all Rex elements were highlighted (Fig. 2). For Hypostomus iheringii (Regan, 1908), no hybridization signal of Rex elements was identified in the heterochromatic block of the chromosome pair 5 (Fig. 3).

Fig. 1
Metaphases of the Harttia species submitted to FISH with probes of the Rex elements. The numbers indicate chromosomal pairs in highlighted. Bar = 10 μm.

Fig. 2
Metaphases of the Harttia species submitted to FISH with probes of the Rex elements. The numbers indicate chromosomal pairs in highlighted. Bar = 10 μm.

Fig. 3
Metaphases of the Hypostomus species submitted to FISH with probes of the Rex elements. The numbers indicate chromosomal pairs in highlighted. Bar = 10 μm.

Discussion

Comparative analysis of the elements Rex of H. kronei and H. nigromaculatus with sequences deposited in the GenBank database revealed a greater similarity of these sequences with species belonging to Loricariidae and other fish families (Tab. 2). The Rex1 sequence presents similarities between phylogenetically distant species (Volff et al., 2000), as verified for Rex1, Rex3 and Rex6 (Mazzuchelli et al., 2009; Borba et al., 2013). In this way, we observed that the three retroelements analyzed are present in several groups of fish and maintain high similarity in their sequences.

In most cases described, the Rex retroelements are preferentially accumulated in heterochromatic portions (Fischer et al., 2004; Da Silva et al., 2002; Bouneau et al., 2003; Ozouf-Costaz et al., 2004). However, just as it were found for other species of Loricariidae (Ferreira et al., 2011b; Pansonato-Alves et al., 2013; Silva et al., 2014; Favarato et al., 2016), the data of this study highlight the location of these elements in both heterochromatic and euchromatic regions of the genome. This feature appears to be a common characteristic of the species belonging to this family.

In H. longipinna, there is a conspicuous heterochromatic block allocated in the acrocentric pair 23 (Blanco et al., 2012a), in which it was not detected the presence of any of the retroelements tested, as well as in the supernumerary chromosomes of this species. The absence of the elements Rex in the B chromosomes of H. longipinna discards the role of these retrotransposons in the origin of these accessory chromosomes. Still, it is possible to infer the probable origin of these B chromosomes from this acrocentric pair. This hypothesis is based on two facts: (i) these RTEs are shared by all Loricariidae previously analyzed (Ferreira et al., 2011b; Pansonato-Alves et al., 2013; Silva et al., 2014; Favarato et al., 2016) and Hypostomus (analyzed in this study), therefore, the invasion in the genome of Harttia is prior to the emergence of the clade and; (ii) the pair 23 is the only chromosome pair free from invasion of the Rex elements in this species. In H. torrenticola, was not detected the presence of Rex elements tested in the heterochromatic block in the terminal position of the long arm of the largest acrocentric pair 22 (Blanco et al., 2013).

The absence of Rex elements in specific heterochromatic regions is not exclusivity of Harttia. In H. iheringii, there is a conspicuous heterochromatic block allocated in the long arm of the submetacentric pair 5, block involved in a possible process of heterochromatinization and evidenced under the polymorphic condition (Traldi et al., 2012). In the individual analyzed (heterozygous for the heterochromatic block), the presence of the retroelements tested was not detected in the heterochromatic region of the chromosome carrying the block.

Considering the genomic invasion by Rex elements prior to the division of the clades within Loricariidae, the association between heterochromatic blocks and the absence of Rex elements in some heterochromatic portions of Harttia and Hypostomus species allows us to assume that the compartmentalized heterochromatin of these blocks prevented the dispersion of retroelements in these chromosomal regions. However, the possible existence of a small amount of retroelements in these regions cannot be disregarded, making it impossible to detect by FISH, as it is proposed for a heterochromatic block allocated in pair 2 of Hypancistrus cf. debilittera (Silva et al., 2014), which does not display the sequence of retrotransposon Rex3.

The analyses with nuclear and mitochondrial molecular markers, showed a close proximity between H. carvalhoi and H. torrenticola, to the point that these species represent a monophyletic clade (Costa-Silva, 2009). Posteriorly, this proximity between the two species was confirmed through chromosomal markers (Blanco et al., 2013). These authors attribute to the centric fission of the largest metacentric pair, which was shared only between these two species, as the event responsible for the origin of the system of sex chromosomes XX/XY₁Y₂ present in H. carvalhoi. The FISHs revealed an accumulation of elements Rex1, Rex3 and Rex6 in the heterochromatic and pericentromeric region of the largest metacentric pair in H. carvalhoi (X chromosome) and the absence of these elements in the largest metacentric pair of H. torrenticola (pair 1). Considering the fact that TEs can be considered hot spots for rearrangements (Valente et al., 2011), the presence of such retroelements in the pericentromeric region of the X chromosome of H. carvalhoi may have aided in the fission that culminated in the formation of chromosomes Y₁ and Y₂; however, it cannot be ruled out the invasion of these RTEs after the emergence of the multiple sex chromosomes system.

The retroelement Rex1 revealed the largest accumulation in pair 15 of H. ancistroides and in pairs 2 and 30 of H. nigromaculatus (Pansonato-Alves et al., 2013). However, for these species, in this study, the accumulation was not directed only to these pairs. In addition, the results observed indicate a greater accumulation of this sequence in these species. Thus, we observed the occurrence of population variations of this marker for these species.

Rex elements have been undergoing some rearrangement processes, some of which identified as recent events (Ferreira et al., 2011a). The dispersed pattern of elements Rex1, Rex3 and Rex6 found for the species analyzed in this study was also found in groups that present a wide chromosomal variety such as in Erythrinus erythrinus (Bloch, Schneider, 1801) (Cioffi et al., 2010) and species of the Hypoptopomatinae family (Ferreira et al., 2011b). On the other hand, in groups that present a sharper conservation on the karyotypic macrotexture, such as cichlids, these retroelements are allocated preferentially in the centromeric and telomeric region of most chromosomes (Valente et al., 2011). This difference in the distribution of TEs, here represented by Rex elements, is possibly related to a number of copies of these sequences in the genome of different species. Whereas the retroelements present a significant influence on chromosomal evolution for being often associated with chromosomal rearrangements (Raskina et al., 2008), the dispersed distribution of Rex retroelements combined with their abundances in the genome of the species studied here can possibly be related with the karyotypic diversity found in Loricariidae.

Studies with repetitive elements dispersed in genomes already demonstrated that they, after the invasion, tend to be silenced and undergo molecular deterioration until they are incorporated into the host genome (Fernández-Medina et al., 2012). In the molecular deterioration phase, the element becomes inactivated and progressively accumulates mutations, insertions and deletions in neutral rates up to completely lose its identity or be lost from the host genome (Fernández-Medina et al., 2012). We verified that the deterioration of the elements dispersed transforms these copies in neutral sequences in the genome, and they may serve as raw material to the domestication by the host genome (Miller et al., 1997). The concept of molecular domestication was used to describe the process where a TE sequence has a co-option to perform a function different from the original for which it was selected and bring benefits to the host genome (Miller et al., 1997). In fact, copies of truncated TE elements can modulate the gene expression in the host genome by providing new regulatory sites, alternatives to “splice” sites, signs of polyadenylation, new binding sites of transcription factors as well as post-transcriptional regulation and the translation regulation (Marino-Ramirez et al., 2005; Muotri et al., 2007; Polavarapu et al., 2008). In addition, it has been shown that numerous genes for microRNAs derive from TEs (Piriyapongsa et al., 2007). Thus, the intense invasion of the elements of the Rex family in Harttia and Hypostomus, demonstrated by the physical location of these elements with the accumulation in euchromatic regions, can represent new genomic and evolutionary alternatives, acting in the adaptation and differentiation of these species.

The transposable elements due to their mobility in the genome have a significant influence on chromosomal evolution because they are often associated with chromosomal rearrangements. In this context the presence of retroelements in some chromosomal regions suggest their participation in various chromosomal rearrangements. In addition, after the invasion on a host, the transposable elements can undergo the molecular domestication process, having a co-option to perform a function different from the original for which it was selected, generating benefits for the host genome. Thus, the intense accumulation of Rex1, Rex3 and Rex6 in all species of Harttia and Hypostomus especially in euchromatic regions can be indicative of the participation of these elements in the diversification and evolution of these species by the acquisition of new functions

Acknowledgments

The authors are grateful to Luis H. da Silva, Pedro L. Gallo, and Antônio D. da Silva for help with the sampling and technical support. This study was financed by FAPESP (Fundacão de Amparo à Pesquisa do Estado de São Paulo), CAPES (Coordenacão de Aperfeicoamento de Pessoal de Nível Superior), Fundação Araucária (Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Estado do Paraná), and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico).

References

• Alves AL, Oliveira C, Foresti F. Karyotype variability in eight species of the subfamilies Loricariinae and Ancistrinae (Teleostei, Siluriformes, Loricariidae). Caryologia. 2003; 56(1):57-63.
• Biscotti MA, Olmo E, Heslop-Harrison JS. Repetitive DNA in eukaryotic genomes. Chromosome Res. 2015; 23(3):415-20.
• Bitencourt JA, Affonso PRAM, Giuliano-Caetano L, Carneiro PLS, Dias AL. Population divergence and peculiar karyoevolutionary trends in the loricariid fish Hypostomus aff. unae from northeastern Brazil. Genet Mol Res. 2012; 11(2):933-43.
• Blanco DR, Vicari MR, Artoni RF, Traldi JB, Moreira-Filho O. Chromosomal characterization of armored catfish Harttia longipinna (Siluriformes, Loricariidae): first report of B Chromosomes in the genus. Zool Sci. 2012a; 29(9):604-09.
• Blanco DR, Bertollo LAC, Lui RL, Vicari MR, Margarido VP, Artoni RF, Moreira-Filho O. A new technique for obtaining mitotic chromosome spreads from fishes in the field. J Fish Biol. 2012b; 81(1):351-57.
• Blanco DR, Vicari MR, Lui RL, Bertollo LAC, Traldi JB, Moreira-Filho O. The role of the Robertsonian rearrangements in the origin of the XX/XY₁Y₂ sex chromosome system and in the chromosomal differentiation in Harttia species (Siluriformes, Loricariidae). Rev Fish Biol Fish. 2013; 23(1):127-34.
• Blanco DR, Vicari MR, Lui RL, Artoni RF, Almeida MC, Traldi JB, Margarido VP, Moreira-Filho O. Origin of the X₁X₁X₂X₂/X₁X₂Y sex chromosome system of Harttia punctata (Siluriformes, Loricariidae) inferred from chromosome painting and FISH with ribosomal DNA markers. Genetica. 2014; 142(2):119-26.
• Blanco DR, Vicari MR, Lui RL, Traldi JB, Bueno V, Martinez JF, Brandão H, Oyakawa O, Moreira-Filho O. Karyotype diversity and evolutionary trends in armored catfish species of the genus Harttia (Siluriformes, Loricariidae). Zebrafish. 2017; 14(2):169-76.
• Borba RS, da Silva EL, Parise-Maltempi PP. Chromosome mapping of retrotransposable elements Rex1 and Rex3 in Leporinus Spix, 1829 species (Characiformes: Anostomidae) and its relationships among heterochromatic segments and W sex chromosome. Mob Genet Elem. 2013; 3(6):e274660.
• Bouneau L, Fisher C, Ozouf-Costaz C, Froschauer A, Jaillon O, Coutanceau JP, et al An active Non-LTR retrotransposon with tandem structure in the compact genome of the pufferfish Tetraodon nigroviridis Genome Res. 2003; 13(7):1686-95.
• Capy P, Bazin C, Higuet D, Langin T. Dynamics and evolution of transposable elements. Austin: Landes Bioscience; 1998.
• Carducci F, Barucca M, Canapa A, Biscotti MA. Rex retroelements and Teleost genomes: An overview. Int J Mol Sci. 2018; 19(11):e3653.
• Centofante L, Bertollo LAC, Moreira-Filho O. Cytogenetic characterization and description of an XX/XY₁Y₂ sex chromosome system in catfish Harttia carvalhoi (Siluriformes, Loricariidae). Cytogen Genome Res . 2006; 112(3-4):320-24.
• Cereali SS, Pomini E, Rosa R, Zawadzki CH, Froenlich O, Giluiano-Caetano L. Karyotype of two species of Hypostomus (Siluriformes, Loricariidae) of the Planalto da Bodoquena, Brazil. Genet Mol Res . 2008; 7(3):583-91.
• Cioffi MB, Martins C, Bertollo LAC. Chromosome spreading of associated transponable elements and robossomal DNA in the fish Erythrinus erythrinus Implications for genome change and karyoevoltion in fish. BMC Evol Biol. 2010; 10(271):1-9.
• Costa-Silva GJ. Análise filogenética entre gêneros da subfamília Loricariinae (Siluriformes: Loricariidae) com ênfase no gênero Harttia, baseada em caracteres moleculares. [MSc dissertation]. Botucatu, SP: Universidade Estadual de São Paulo; 2009.
• Favarato RM, da Silva M, de Oliveira RR, Artoni RF, Feldberg E, Matoso DA. Cytogenetic diversity and the evolutionary dynamics of rDNA genes and telomeric sequences in the Ancistrus genus (Loricariidae: Ancistrini). Zebrafish . 2016; 13(2):103-11.
• Fernández-Medina RD, Ribeiro JMC, Carareto CMA, Velasque L, Struchiner CJ. Losing identity: structural diversity of transposable elements belonging to different classes in the genome of Anopheles gambiae BMC Genomics. 2012; 13(272):1-15.
• Ferreira DC, Porto-Foresti F, Oliveira C, Foresti F. Transposable elements as a potential source for understanding the fish genome. Mob Genet. Elem 2011a; 1(2):112-17.
• Ferreira DC, Oliveira C, Foresti F. Chromosome mapping of retrotransposable elements Rex1 and Rex3 in three fish species in the subfamily Hypoptopomatinae (Teleostei, Siluriformes, Loricariidae). Cytogenet Genome Res . 2011b; 132(1-2):64-70.
• Fischer C, Bouneau L, Coutenceau JP, Weissenbach J, Vollf JN, Ozouf-Costaz C. Global heterochromatic colocalization of transposable elements with minisatellites in the compact genome of the pufferfish Tetraodon nigroviridis Gene. 2004; 336(2):175-83.
• Foresti F, Oliveira C, Almeida-Toledo LF. A method for chromosome preparations from large specimens of fishes using ‘in vitro” short treatment with colchicine. Experientia. 1993; 49(9):810-13.
• Fricke R, Eschmeyer WN, Fong JD. Species by subfamily/subfamily [Internet]. San Francisco: California Academy of Science; 2019. Available from: http://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp
  » http://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp
• Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 1999; 41:95-98.
• Hartl DL, Lozovsaya ER, Lawrence JG. Nonautonomous transposable elements in prokaryotes and eukaryotes. Genetica . 1992; 86(1-3):47-53.
• Kavalco KF, Pazza R, Bertollo LAC, Moreira-Filho O. Karyotypic diversity and evolution of Loricariidae (Pisces, Siluriformes). Heredity. 2005; 94(2):180-86.
• Mariño-Ramirez L, Lewis KC, Landsman D, Jordan IK. Transposable elements donate lineage-specific regulatory sequences to host genomes. Cytogenet Genome Res. 2005; 110(1-4):333-41.
• Mazzuchelli J, Martins C. Genomic organization of repetitive DNAs in the cichlid fish Astronotus ocellatus Genetica . 2009; 136(3):461-69.
• Miller WJ, McDonald JF, Pinsker W. Molecular domestication of mobile elements. Genetica . 1997; 100:261-70.
• Muotri AR, Marchetto MC, Coufal NG, Gage FH. The necessary junk: new functions for transposable elements. Hum Mol Genet. 2007; 16(2):159-67.
• Muramoto J, Ohno S, Atkin NB. On the diploid state of the fish order Ostariophysi. Chromosoma. 1968; 24(1):59-66.
• Ozouf-Costaz C, Brandt J, Körting C, Pisano E, Bonillo C, Coutanceau J-P et al Genome dynamics and chromosomal localization of the non-LTR retrotransposons Rex1 and Rex3 in Antarctic fish. Antarctic Sci. 2004; 16(1):51-57.
• Pansonato-Alves JC, Serrano EA, Utsunomia R, Scacchetti PC, Oliveira C, Foresti F. Mapping five repetitive DNA classes in sympatric species of Hypostomus (Teleostei: Siluriformes: Loricariidae): analysis of chromosomal variability. Rev Fish Biol Fish . 2013; 23(4):477-89.
• Pinkel D, Straume T, Gray JW. Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci USA. 1986; 83(9):2934-38.
• Piriyapongsa J, Mariño-Ramirez L, Jordan IK. Origin and evolution of human microRNAs from transposable elements. Genetics. 2007; 176(2):1323-37.
• Polavarapu N, Mariño-Ramirez L, Landsman D, McDonald JF, Jordan IK. Evolutionary rates and patterns for human transcription factor binding sites derived from repetitive DNA. BMC Genomics 2008; 9:226.
• Raskina O, Barber JC, Nevo E, Belyayev A. Repetitive DNA and chromosomal rearrangements: speciation-related events in plant genomes. Cytogenet Genome Res . 2008; 120(3-4):351-57.
• Rodrigues RM. Estudos cromossômicos e moleculares em Loricariinae com ênfase em especies de Rineloricaria (Siluriformes, Loricariidae): uma perspective evolutiva. [MSc dissertation] . Universidade de São Paulo; 2010.
• Sambrook J, Maniatis T, Fritsch EF. Molecular cloning: A laboratory manual. New York: Laboratory Press; 2001.
• Schneider CH, Gross MC, Terencio ML, Carmo EJ, Martins C, Feldberg E. Evolutionary dynamics of retrotransposable elements Rex1, Rex3 and Rex6 in neotropical cichid genomes. BMC Evol Biol . 2013; 13(152):1-15.
• da Silva C, Hadji H, Ozouf-Costaz C, Nicaud S, Jaillon O, Weissenbrach J, Crollius HR. Remarkable compartmentalization of transposable elements and pseudogenes in the heterochromatin of the Tetraodon nigroviridis genome. Proc Natl Acad Sci USA . 2002; 99(21):1636-41.
• da Silva M, Ribeiro ED, Matoso DA, Sousa LM, Hrbek T, Rapp Py-Daniel L, et al Chromosomal polymorphism in two species of Hypancistrus (Siluriformes: Loricariidae): an integrative approach for understanding their biodiversity. Genetica . 2014; 142:127-39.
• Teixeira WG, Ferreira IA, Cabral-de-Mello DC, Mazzuchelli J, Valente GT, Pinhal D, et al Organization of repeated DNA elements in the genome of the cichlid fish Cichla kelberi and its contributions to the knowledge of fish genomes. Cytogen Genome Res. 2009; 125(3):224-34.
• Traldi JB, Vicari MR, Blanco DR, Martinez JF, Artoni RF, Moreira-Filho O. First karyotype description of Hypostomus iheringii (Regan, 1908): a case of heterochromatic polymorphism. Comp Cytogen. 2012; 6(2):115-25.
• Traldi JB, Blanco DR, Vicari MR, Martinez JF, Lui RL, Barros AV, Artoni RF, Moreira-Filho O. Chromosomal diversity in Hypostomus (Siluriformes, Loricariidae) with emphasis on physical mapping of 18S and 5S rDNA sites. Gen Mol Res. 2013a; 12(1):463-71.
• Traldi JB, Blanco DR, Vicari MR, Martinez JF, Lui RL, Artoni RF, Moreira-Filho O. Physical mapping of (GATA)_n and (TTAGGG)_n sequences in species of Hypostomus (Siluriformes, Loricariidae). J Genet. 2013b; 92(1):127-30.
• Valente GT, Mazzuchelli J, Ferreira IA, Poletto AB, Fantinatti BEA, Martins C. Cytogenetic mapping of the retroelements Rex1, Rex3 and Rex6 among cichlid fish: new insights on the chromosomal distribution of transposable elements. Cytogen Genome Res . 2011; 133(1):34-42.
• Volff JN, Körting C, Froschauer A, Sweeney K, Schartl M. Non-LTR retrotransposons encoding a restriction enzyme-like endonuclease in vertebrates. J Mol Evol. 2001; 52(4):351-60.
• Volff JN, Körting C, Schartl M. Multiple lineages of the non-LTR retrotransposon Rex1 with varying success in invading fish genomes. Mol Biol Evol. 2000; 17(11):1673-84.
• Volff JN, Körting C, Sweeney K, Schartl M. The non-LTR retrotransposon Rex3 from the fish Xiphophorus is widespread among teleosts. Mol Biol Evol . 1999; 16(11):1427-38.
• Zawadzki CH, Weber C, Pavanelli CS. A new dark-saddled species of Hypostomus (Siluriformes: Loricariidae) from the upper Paraguay River basin. Neotrop Ichthyol. 2010; 8(4):719-25.

• ERRATA

  In the article “Chromosomal distribution of the retroelements Rex1, Rex3 and Rex6 in species of the genus Harttia and Hypostomus (Siluriformes: Loricariidae)”, with DOI: 10.1590/1982-0224-20190010, published in the journal Neotropical Ichthyology, 17(2): e190010, page e190010[3], Tab. 2:
  Where read:Hypostomus nigromaculatus Rex6 549pb MH595480
  Should read:Hypostomus nigromaculatus Rex6 549pb MH595489
  All changes are already incorporated in the online PDF and HTML versions of these articles available at http://www.scielo.br/ni
  Neotropical Ichthyology, 17(3): e1902er, September 2019

Edited by

Claudio Oliveira

Data availability

Data citations

Fricke R, Eschmeyer WN, Fong JD. Species by subfamily/subfamily [Internet]. San Francisco: California Academy of Science; 2019. Available from: http://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp

Publication Dates

• Publication in this collection
  18 July 2019
• Date of issue
  2019

History

• Received
  01 Feb 2019
• Accepted
  12 June 2019