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. 2012 Aug 1;2(8):931–941. doi: 10.1534/g3.112.003467

Satellite DNA-Like Elements Associated With Genes Within Euchromatin of the Beetle Tribolium castaneum

Josip Brajković *, Isidoro Feliciello *,†, Branka Bruvo-Mađarić *, Đurđica Ugarković *,1
PMCID: PMC3411249  PMID: 22908042

Abstract

In the red flour beetle Tribolium castaneum the major TCAST satellite DNA accounts for 35% of the genome and encompasses the pericentromeric regions of all chromosomes. Because of the presence of transcriptional regulatory elements and transcriptional activity in these sequences, TCAST satellite DNAs also have been proposed to be modulators of gene expression within euchromatin. Here, we analyze the distribution of TCAST homologous repeats in T. castaneum euchromatin and study their association with genes as well as their potential gene regulatory role. We identified 68 arrays composed of TCAST-like elements distributed on all chromosomes. Based on sequence characteristics the arrays were composed of two types of TCAST-like elements. The first type consists of TCAST satellite-like elements in the form of partial monomers or tandemly arranged monomers, up to tetramers, whereas the second type consists of TCAST-like elements embedded with a complex unit that resembles a DNA transposon. TCAST-like elements were also found in the 5′ untranslated region (UTR) of the CR1-3_TCa retrotransposon, and therefore retrotransposition may have contributed to their dispersion throughout the genome. No significant difference in the homogenization of dispersed TCAST-like elements was found either at the level of local arrays or chromosomes nor among different chromosomes. Of 68 TCAST-like elements, 29 were located within introns, with the remaining elements flanked by genes within a 262 to 404,270 nt range. TCAST-like elements are statistically overrepresented near genes with immunoglobulin-like domains attesting to their nonrandom distribution and a possible gene regulatory role.

Keywords: repetitive DNA, satellite DNA, gene regulation, transposon, immunoglobulin-like genes

Based on the hypothesis of Britten and Davidson (1971), repetitive elements can be a source of regulatory sequences and act to distribute regulatory elements throughout the genome. In particular, mobile transposable elements (TEs) are predicted to be a source of noncoding material that allows for the emergence of genetic novelty and influences evolution of gene regulatory networks (Feschotte 2008). Recently it has been shown that at least 5.5% of conserved noncoding elements unique to mammals originate from mobile elements and are preferentially located close to genes involved in development and transcription regulation (Lowe et al. 2007). The complete sequence conservation, wide evolutionary distribution, and presence of functional elements such as promoters and transcription factor binding sites within some satellite DNA sequences has led to the assumption that in addition to participating in centromere formation, they might also act as cis-regulatory elements of gene expression (Ugarković 2005). To perform potential regulatory functions, satellite DNA elements are predicted to be preferentially distributed in euchromatic portion of the genomes in the vicinity of genes. Whole-genome sequencing projects enable the presence and distribution of satellite DNA repeats in the euchromatic portion of the genome to be determined. The analysis of satellite DNA-like elements dispersed within euchromatin, and their comparison with homologous elements present within heterochromatin, also may reveal insights into the origin of satellite DNAs and their subsequent evolution (Kuhn et al. 2012).

Satellite DNAs are major building elements of pericentromeric and centromeric heterochromatin in many eukaryotic species, and in certain species they account for the majority of genomic DNA, as in beetles from the coleopteran family Tenebrionidae (Ugarković and Plohl 2002). In the red flour beetle Tribolium castaneum, pericentromeric heterochromatin comprises approximately 40% of the genome, and TCAST satellite DNA has previously been characterized as the major satellite that encompasses centromeric as well as pericentromeric regions of all 20 chromosomes (Ugarković et al. 1996). TCAST satellite is composed of two subfamilies, Tcast1a and Tcast1b, which together comprise 35% of the whole genome. Tcast1a and Tcast1b have an average homology of 79% and are a similar size at 362 bp and 377 bp, respectively, but they are characterized by a divergent, subfamily specific region of approximately 100 bp (Feliciello et al. 2011). The genome sequencing project of T. castaneum has recently been completed (Richards et al. 2008). Sequencing involved the euchromatic portion of the genome, with >20% of the genome, corresponding to heterochromatic regions, excluded due to technical difficulties.

In this article, we searched for the presence of TCAST satellite-homologous elements within the assembled T. castaneum genome by using a comprehensive computational analysis. By searching the sequenced T. castaneum genome, we found 68 TCAST satellite DNA arrays within the euchromatin of all chromosomes. They were mapped to 5′ or 3′ ends, as well as within introns, of more than 100 protein-coding genes. Based on sequence characteristics, dispersed TCAST-like elements were classified into two groups. The first group includes partial TCAST satellite monomers or short arrays of tandemly arranged monomers up to tetramers. The second group contains TCAST-like element embedded within complex repeat units that contain two hallmarks of DNA transposons, terminal inverted repeats and target-size duplications. The evolutionary relationship and possible modes of dispersion of the two types of dispersed TCAST-like sequences are discussed. In addition, we examined the sequence divergence, phylogenetic relationship, and chromosomal distribution of the elements. Annotation, characterization, and classification of genes within the region of TCAST-like elements are reported, with the preferential localization of TCAST-like elements near specific groups of genes identified. Our results demonstrate for the first time, the enrichment of satellite DNA-like elements in the vicinity of genes with immunoglobulin-like domains and suggest their possible gene-regulatory role.

Materials and Methods

BLASTN version 2.2.22+ was used to screen the NCBI refseq_genomic database of T. castaneum. All scaffolds that have not been mapped to linkage groups were also screened. The program was optimized to search for highly similar sequences (megablast) to the query sequence [TCAST consensus sequence (Ugarković et al. 1996)]. Genes flanking TCAST–homologous elements were found automatically by NCBI blast. Sequences corresponding to hits, as well as their flanking regions, were analyzed by dot plot (http://www.vivo.colostate.edu/molkit/dnadot/), using standard parameters (window size 9, mismatch limit 0), or more relaxed conditions (window size 11, mismatch limit 1), to determine the exact start and end site of specific TCAST-like elements. The TCAST transposon-like elements were analyzed in detail for the presence of hallmarks such as terminal inverted repeats (TIRs) and target-site duplications with the aid of the Gene Jockey sequence analysis program (for Apple Macintosh). Secondary structures were determined using the default parameters of the MFOLD program available online [http://mfold.rna.albany.edu/?q=mfold (Zuker 2003)]. AT content was analyzed using BioEdit Sequence Alignment Editor (Hall 1999). Repbase, a reference database of eukaryotic repetitive DNA, was screened using WU-BLAST (Kohany et al. 2006).

Sequence alignment was performed using MUSCLE algorithm (Edgar 2004) combined with manual adjustment. All sequences were included in the alignment, with the exception of the ones that did not at least partially overlap with other sequences. Gblocks was used to eliminate poorly aligned positions and divergent regions of the alignments (Talavera and Castresana 2007). Alignments (original fasta files) are available upon request. jModelTest 0.1.1 software (Posada 2008) was used to infer best-fit models of DNA evolution—TPM3uf+G for transposon-like and A type elements and TPM1uf for B type elements. Maximum likelihood (ML) trees were estimated with the PhyML 3.0 software (Guindon and Gascuel 2003) using best-fit models. Markov chain Monte Carlo Bayesian searches were performed in MrBayes v. 3.1.2. (Huelsenbeck and Ronquist 2001) under the best-fit models (two simultaneous runs, each with four chains; 3 × 106 generations; sampling frequency one in every 100 generations; majority rule consensus trees constructed based on trees sampled after burn-in). Branch support was evaluated by bootstrap analysis (1000 replicates) in ML and by posterior probabilities in Bayesian analyses. Pairwise sequence diversity (uncorrected P) was calculated using the MEGA 5.05 software (Tamura et al. 2011).

T. castaneum gene homologs in Drosophila melanogaster were searched using the OrthoDB Phylogenomic database. Each gene has OrthoDB identificator, with Uniprot data linked to OrthoDB (Waterhouse et al. 2011). To find sets of biological annotations that frequently appear together and are significantly enriched in a set of genes located near TCAST-like elements, program GeneCodis 2.0 available online (http://genecodis.dacya.ucm.es/) was used. GeneCodis generates statistical rank scores for single annotations and their combinations. To find all the possible combinations of annotations, GeneCodis uses the apriori algorithm introduced by Agrawal et al. 1993. Once the annotations were extracted, a statistical analysis based on the hypergeometric distribution or the χ2 test of independence was executed to calculate the statistical significance (P values) for each individual annotation or co-annotations.

Two-tailed hypergeometric test with Bonferroni correction (alpha = 0.025) was used to analyze the distribution of TCAST-like elements among T. castaneum chromosomes. In each chromosome the frequency of TCAST-like elements was compared with the frequency in the complete sample and the significance of deviations was calculated.

Results

Identification of dispersed TCAST-like elements

Using the consensus sequence of TCAST satellite DNA (Ugarković et al. 1996) as a query sequence, we screened the NCBI refseq_genomic database of T. castaneum with the alignment program BLASTN version 2.2.22+. The program was optimized to search for highly similar sequences (megablast) and blast hits on the query sequence were analyzed individually. Alignments were mapped regarding start and end site, chromosome number, and total length. When the distance between two alignments on the same chromosome was short, the genomic sequence was further analyzed by dot plot to identify any potential continuity between the two alignments. Only genomic sequences with at least 140 nt (40% of TCAST monomer length) of continuous sequence and >80% identity to the TCAST consensus sequence were considered for further analysis. The total number of dispersed TCAST-like elements was 68, with 36 elements flanked by genes at both 5′ and 3′ ends, 3 elements flanked by a single gene either at 5′ or 3′ end (sequences no. 36, 39, 50), and the 29 elements positioned within introns (Table 1). Except 68 TCAST-like elements associated with genes, no other dispersed TCAST-like elements were found within the assembled T. castaneum genome. Analysis of scaffolds that have not been mapped to linkage groups revealed the presence of an additional 41 TCAST-like elements, but because they were not mapped to T. castaneum genome and could possibly derive from heterochromatin, we did not consider them for further analysis.

Table 1. TCAST-like elements associated with genes within T. castaneum euchromatin.

Uniprot Entrez Gene Name Chr Sat_seq. Position Distance, bp DM Homolog FBgn Type Length Copies
D6WZP1 662564 Altered disjunction 9 1 5′ 18,773 Q9VEH1 FBgn0000063 Satellite 734 2.0
D6WZP3 662624 Ras-related protein Rab-26 9 1 3′ 7795 Q9VP48 FBgn0086913 Satellite 734 2.0
D6WZL9 661947 Probable serine/threonine-protein kinase 9 2 Inside Q0KHT7 FBgn0052666 Satellite 993 2.8
D6X226 660275 Arrest 9 3 5′ 99,669 Q8IP89 FBgn0000114 Satellite 716 2.0
D6X238 661741 Numb 9 3 3′ 115,984 P16554 FBgn0002973 Satellite 716 2.0
100141832 no match on uniprot 9 4 5′ 1520 Satellite 517 1.4
D6X2D0 660440 Short-chain dehydrogenase 9 4 3′ 6704 Q9VE80 FBgn0038610 Satellite 517 1.4
D6X1E7 656884 Cytochrome P450 306A1 9 5 5′ 404,270 Q9VWR5 FBgn0004959 Satellite 1058 2.9
D6X2U7 656977 Elongase 9 5 3′ 9947 Q9VCY6 FBgn0038986 Satellite 1058 2.9
D6X2C4 660195 Dopamine receptor 1 9 6 Inside P41596 FBgn0011582 Satellite 304 0.8
D6X2U7 656977 Elongase 9 7 5′ 7128 Q9VCY6 FBgn0038986 Satellite 394 1.1
D6X366 657055 elongation of very long chain fatty acids protein 9 7 3′ 50,111 Q9VCY5 FBgn0053110 Satellite 394 1.1
D6X0D7 657748 Ret oncogene 9 8 5′ 56,625 Q8INU0 FBgn0011829 Satellite 213 0.6
D6X0E1 657829 Dpr9 9 8 3′ 62,781 Q9VFD9 FBgn0038282 Satellite 213 0.6
D6X2H8 654954 ADAM metalloprotease 9 9 Inside Q6QU65 FBgn0051314 Transposon 1107
D6X2U7 655561 Elongase 9 10 5′ 47,902 Q9VCZ0 FBgn0038983 Transposon 1085
D6X2V3 655640 Putative uncharacterized protein 9 10 3′ 67,953 Q9VDB7 FBgn0038881 Transposon 1085
D6X244 655011 Serine/threonine-protein kinase 32B 9 11 Inside Q0KID3 FBgn0052944 Transposon 1062
D6X374 100141521 Putative uncharacterized protein 9 12 Inside Q9VGZ4 FBgn0037814 Satellite 292 0.8
D6X2C4 660195 Dopamine receptor 1 9 13 Inside P41596 FBgn0011582 Transposon 900
D6X259 656290 Transport and Golgi organization 13 9 14 5′ 9456 Q9VGT8 FBgn0040256 Satellite 222 0.6
D6X260 656373 Protein-tyrosine sulfotransferase 9 14 3′ 33,523 Q9VYB7 FBgn0086674 Satellite 222 0.6
D6X075 658603 MICAL-like protein 9 15 5′ 39,684 Q9VU34 FBgn0036333 Satellite 203 0.6
D6X1P2 658891 tiptop 9 15 3′ 142,821 Q9U3V5 FBgn0028979 Satellite 203 0.6
D6X095 659195 Troponin C 9 16 5′ 3922 P47947 FBgn0013348 Transposon 589
D6X0I1 659336 Troponin C 9 16 3′ 15,143 P47947 FBgn0013348 Transposon 589
D6X1J0 655713 Transporter 9 17 Inside Q9NB97 FBgn0034136 Satellite 915 2.5
D6WF56 100141877 zinc finger protein 250 3 18 5′ 125,685 Q7KAH0 FBgn0027339 Satellite 1208 3.4
D6WF61 656924 Transcription initiation factor TFIID subunit 7 3 18 3′ 64,294 Q9VHY5 FBgn0024909 Satellite 1208 3.4
D6WGB1 659040 Mahya 3 19 5′ 115,537 P20241 FBgn0002968 Satellite 687 1.9
D6WGB5 659201 V-type proton ATPase subunit E 3 19 3′ 82,217 P54611 FBgn0015324 Satellite 687 1.9
D6WII0 100141571 NADH dehydrogenase, putative 3 20 5′ 4278 Q9W3N7 FBgn0029971 Transposon 635
D6WII2 100142263 Putative uncharacterized protein 3 20 3′ 18,585 Q9VIY1 FBgn0032769 Transposon 635
D6WFT8 657535 WD repeat-containing protein 47 3 21 Inside Q960Y9 FBgn0026427 Satellite 604 1.7
D6WDY2 656125 Kynurenine aminotransferase 3 22 5′ 10,696 Q8SXC2 FBgn0037955 Transposon 1000
D6WDY4 656298 Annexin IX 3 22 3′ 11,599 P22464 FBgn0000083 Transposon 1000
D6WFK8 656174 ankyrin 2,3/unc44 3 23 Inside Q7KU95 FBgn0085445 Transposon 1081
D6WFX1 657874 ral guanine nucleotide exchange factor 3 24 5′ 64,025 Q8MT78 FBgn0034158 Transposon 888
D6WFX3 658031 galactose-1-phosphate uridylyltransferase 3 24 3′ 3958 Q9VMA2 FBgn0031845 Transposon 888
D6WDQ4 659233 Putative uncharacterized protein 3 25 5′ 15,051 Q8T0R9 FBgn0038809 Transposon 1016
D6WDQ6 659376 coiled-coil domain containing 96 3 25 3′ 9162 A1ZA72 FBgn0013988 Transposon 1016
D6WF68 655042 glucose dehydrogenase 3 26 5′ 25,896 Q9VY00 FBgn0030598 Transposon 1067
C3XZ92 655348 Mitogen-activated protein kinase kinase kinase kinase 2 3 26 3′ 92,876 Q8SYA1 FBgn0034421 Transposon 1067
D6WE82 658463 Putative uncharacterized protein 3 27 Inside Q9VDK2 FBgn0038815 Transposon 314
D6WHX6 658191 Putative uncharacterized protein 3 28 5′ 173,881 Q1RKQ9 FBgn0085382 Transposon 826
D6WI58 658343 Cathepsin L 3 28 3′ 82,559 Q95029 FBgn0013770 Transposon 826
D6WDJ9 656922 Putative uncharacterized protein 3 29 5′ 173,548 Q8IPJ1 FBgn0031859 Transposon 1084
D6WDN0 657559 PRMT5 3 29 3′ 383,809 Q9U6Y9 FBgn0015925 Transposon 1084
D6WGS3 656976 Putative uncharacterized protein 3 30 5′ 37572 A0AMQ8 FBgn0034655 Satellite 216 0.6
D6WGT0 100142515 calpain 3 3 30 3′ 226,707 Q11002 FBgn0008649 Satellite 216 0.6
D6WDS8 660532 Muscle-specific protein 300 3 31 5′ 378,626 Q4ABG9 FBgn0260952 Transposon 1060
D6WDT0 654860 Phosphatidylinositol-binding clathrin assembly protein 3 31 3′ 7855 C1C3H4 FBgn0086372 Transposon 1060
D6WHF2 664188 Nephrin 3 32 Inside Q9W4T9 FBgn0028369 Transposon 666
D6WI96 100142620 Heat shock protein 70 3 33 Inside P11147 FBgn0001219 Transposon 1058
D6WG02 654917 N-acetylglucosaminyltransferase vi 3 34 Inside Q9VUH4 FBgn0036446 Transposon 319
D6WYD1 656891 Putative uncharacterized protein 8 35 5′ 385,712 Q8SY79 FBgn0032249 Satellite 625 1.7
D6WYN3 654942 serine-type protease inhibitor 8 35 3′ 58,583 Q9VSC9 FBgn0035833 Satellite 625 1.7
D6WYA1 657913 Copia protein (Gag-int-pol protein) 8 36 3′ 262 B6V6Z8 ?? Satellite 196 0.5
D6WYC9 656718 Cmp-n-acetylneuraminic acid synthase 8 37 Inside B5RJF3 FBgn0052220 Transposon 831
D6WV42 656028 CG5080 8 38 Inside Q7K3E2 FBgn0031313 Transposon 582
D6WYA0 100142507 Beaten path 8 39 5′ 7165 Q94534 FBgn0013433 Transposon 1181
D6WUX6 662235 Putative uncharacterized protein 8 40 Inside Q7KUK9 FBgn0036454 Transposon 440
D6X0E1 654938 defective proboscis extension response 7 41 Inside Q9VFD9 FBgn0038282 Satellite 722 2.0
D6WPX8 662021 Ribosome-releasing factor 2, mitochondrial 7 42 5′ 17,480 Q9VCX4 FBgn0051159 Transposon 905
A2AX72 662058 Gustatory receptor 7 42 3′ 1581 Q9VPT1 FBgn0041250 Transposon 905
D6WTD1 661895 similar to chitinase 6 7 43 Inside Q9W2M7 FBgn0034580 Satellite 1440 4.0
D6WPE6 100142073 voltage-gated potassium channel 7 44 Inside P17970 FBgn0003383 Transposon 814
D2A2C6 663849 Putative uncharacterized protein 4 45 5′ 9489 Q9V3S3 FBgn0013300 Satellite 549 1.5
D2A2D1 663875 Putative uncharacterized protein 4 45 3′ 10,920 Q9W191 FBgn0034994 Satellite 549 1.5
D2A2I0 657017 Putative uncharacterized protein 4 46 5′ 5820 Q8SZ28 FBgn0033786 Satellite 558 1.6
D2A2I1 657098 Ribonucleoside-diphosphate reductase 4 46 3′ 7000 P48591 FBgn0012051 Satellite 558 1.6
D1ZZG6 660983 Kinesin-like protein 4 47 Inside Q9VLW2 FBgn0031955 Transposon 508
D2A2P8 100142595 PiggyBac transposable element 4 48 Inside Q9VHL1 FBgn0037633 Transposon 377
D6WB65 655028 E74 2 49 5′ 60,525 P20105 FBgn0000567 Satellite 770 2.1
D6WB73 654962 organic cation transporter 2 49 3′ 2638 Q7K3M6 FBgn0034479 Satellite 770 2.1
D6WBG8 659129 pre-mRNA-splicing helicase BRR2 2 50 3′ 4811 Q9VUV9 FBgn0036548 Satellite 728
D6WB14 658844 monophenolic amine tyramine 2 51 5′ 7955 P22270 FBgn0004514 Transposon 567
D6WB15 658769 Cuticular protein 47Ef 2 51 3′ 16,173 A1Z8H7 FBgn0033603 Transposon 567
D6WB29 657778 Endoprotease FURIN 2 52 Inside P30432 FBgn0004598 Transposon 1045
A8DIV5 657942 Nicotinic acetylcholine receptor subunit alpha11 2 53 5′ 13,645 P25162 FBgn0004118 Transposon 1021
D6WB29 657778 Endoprotease FURIN 2 53 3′ 4875 P30432 FBgn0004598 Transposon 1021
D6X3I9 661787 Transcription initiation factor IIF 10 54 5′ 10,025 Q05913 FBgn0010282 Satellite 870 2.4
D6X3J1 661827 Putative uncharacterized protein 10 54 3′ 6607 Satellite 870 2.4
D6X4P3 655389 Neutral alpha-glucosidase ab 10 55 Inside Q7KMM4 FBgn0027588 Satellite 694 1.9
D6X3H5 661246 Neurexin-4 10 56 5′ 2234 Q94887 FBgn0013997 Satellite 224 0.6
D6X3H7 661308 Succinate semialdehyde dehydrogenase 10 56 3′ 14,901 Q9VBP6 FBgn0039349 Satellite 224 0.6
D6X4V6 655916 Tubby, putative 10 57 Inside Q9VB18 FBgn0039530 Transposon 763
D6X3J6 662034 Putative uncharacterized protein 10 58 5′ 1015 Q9VEJ9 FBgn0038511 Satellite 564 1.6
D6X3J7 657069 cdc73 domain protein 10 58 3′ 27,239 Q9VHI1 FBgn0037657 Satellite 564 1.6
D2A693 663231 lysine-specific demethylase 4B 6 59 Inside Q9V6L0 FBgn0053182 Satellite 498 1.4
D2A490 659655 Facilitated trehalose transporter Tret1-2 homolog 6 60 Inside Q8MKK4 FBgn0033644 Transposon 689
D2A6I4 659728 Putative uncharacterized protein 6 61 5′ 116,030 Q9W4G2 FBgn0260971 Transposon 764
D2A6I6 659791 Putative uncharacterized protein 6 61 3′ 4860 Q9VNB4 FBgn0037323 Transposon 764
D2A3V0 657272 Fasciclin-3 6 62 5′ 37,286 P15278 FBgn0000636 Satellite 281 0.8
D2A3V3 657421 LIM domain kinase 1 6 62 3′ 21,789 Q8IR79 FBgn0041203 Satellite 281 0.8
D6W8F4 660322 Disco-related x 63 Inside Q9VXJ5 FBgn0042650 Satellite 530 1.5
D6W8D3 659123 PlexA x 64 5′ 1973 O96681 FBgn0025741 Transposon 848
D6WGD2 659272 Aldose-1-epimerase x 64 3′ 6472 Q9VRU1 FBgn0035679 Transposon 848
B3MMG1 657652 Neural-cadherin 5 65 Inside O15943 FBgn0015609 Satellite 273 0.8
D6WNN6 658579 Transient receptor potential-gamma protein 5 66 5′ 2547 Q9VJJ7 FBgn0032593 Transposon 894
A3RE80 658661 Cardioacceleratory peptide receptor 5 66 3′ 27,105 Q868T3 FBgn0039396 Transposon 894
A1JUG2 661207 Ultraspiracle 5 67 Inside P20153 FBgn0003964 Satellite 379 1.1
D6WNB3 656063 Y box protein 5 68 5′ 14,993 O46173 FBgn0022959 Satellite 455 1.3
D6WNB6 656095 Peptide chain release factor 1 5 68 3′ 350,365 Q9VK20 FBgn0032486 Satellite 455 1.3
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A list of genes with gene identity numbers, gene name, chromosomal location, position, and distance relative to the associated TCAST-like element, as well as a list of TCAST-like elements, their types (satellite or transposon-like), total length in bp, and copy number of satellite repeats within an array are shown.

There were only three cases in which two different TCAST-like elements were associated with the same gene: gene D6X2C4 contains TCAST-like sequences no. 6 and 13 within introns, gene D6X2U7 is flanked at 5′ and 3′ end by sequences no. 5 and 7, respectively, whereas gene D6WB29 is located at 3′ end of the sequence no. 53 and has sequence no. 52 within an intron. All other TCAST-like elements were positioned near or within different genes. Thus in total, there were 101 genes found in the vicinity of TCAST-like elements. Characteristics of the genes associated with TCAST-like elements, including gene identity number, gene name and chromosomal location, position relative to the associated TCAST-like element, and distances between TCAST-like elements and genes, are shown in Table 1 Distances between TCAST-like elements and genes range from 262 nt (gene positioned at 3′ site of the sequence no. 36), to a maximal distance of 404,270 nt (gene positioned at 5′ site of the sequence no. 5).

Characteristics of TCAST-like elements

TCAST satellite-like elements:

Sequence analysis of the 68 TCAST-like elements identified within the vicinity of genes enabled their classification into two groups. The first group contains partial TCAST satellite monomers or tandemly arranged elements, either complete or partial dimers, trimers, or tetramers (Table 1). The minimal size of satellite repeat was 203 nt (0.6 of complete TCAST monomer; sequence no. 15), whereas the maximal size was 1440 nt (four complete TCAST monomers; sequence no. 43; Table 1). In many sequences, two subtypes of TCAST satellite monomers were mutually interspersed: Tcast1a and Tcast1b. Tcast1b corresponds to the TCAST satellite consensus that was used as a query sequence (Ugarković et al. 1996), and Tcast1a corresponds to the TCAST subfamily described in Feliciello et al. 2011. Tcast1a and Tcast1b have an average homology of 79% and are of similar sizes at 362 bp and 377 bp respectively, but are characterized by a divergent, subfamily specific region of approximately 100 bp (Feliciello et al. 2011). There were 34 TCAST satellite-like elements found within or in the region of 53 genes. Lengths of TCAST satellite-like elements (Table 1), their exact start and end sites within genomic sequence and composition (supporting information, Table S1) are provided.

To see whether there is any clustering of sequences of TCAST satellite-like elements due to the difference in the homogenization at the level of local array, chromosome, or among different chromosomes, sequence alignment and phylogenetic analysis were performed. Tcast1a and Tcast1b subunits were extracted from TCAST satellite-like sequences and analyzed separately. Alignment was performed on 24 Tcast1a subunits, ranging in size from 136 and 377 bp (File S1). The average pairwise distances between Tcast1a subunits of TCAST satellite-like sequences was 5.8%. Alignment adjustment using Gblocks, which eliminates poorly aligned positions and divergent regions, resulted in few changes; therefore, the original, unadjusted alignment was used for the construction of phylogenetic trees. Because the sequences differ in lengths and comprise regions of divergent variability, methods that take into account specific models of DNA evolution were considered as the most suitable for the construction of phylogenetic trees, ML and Bayesian (Markov chain Monte Carlo). The ML tree showed weak resolution with no significant support for clustering of sequences derived from the same satellite-like array or from the same chromosome. Similarly, the Bayesian tree demonstrated no significant sequence clustering (Figure 1A).

Figure 1 .

Figure 1 

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Bayesian/ML phylogenetic trees of: (A) TCAST satellite-like elements (subunits Tcast1a), (B) TCAST satellite-like elements (subunits Tcast1b), and (C) TCAST transposon-like elements. Sequence numbers correspond to those in Table 1. When a particular sequence is composed of few subrepeats (e.g., Tcast1a or Tcast1b), numbers indicating subrepeats are added (e.g., 43_1, 43_2, 43_3). Numbers in brackets indicate chromosomes on which the corresponding sequences are located. Numbers on branches indicate Bayesian posterior probabilities/ML bootstrap support (above 0.5/50%, respectively).

Alignment of 28 Tcast1b subunits, ranging from 159 bp to 363 bp (File S2), was also not significantly affected by adjustment with Gblocks; therefore, the unadjusted alignment was used for the construction of phylogenetic trees (Figure 1B). The average pairwise divergence between Tcast1b subunits, of TCAST satellite-like sequences, was 6.7%. With the ML phylogenetic tree, four groups composed of two or three sequences, were resolved by relatively low bootstrap values. However, the majority of Tcast1b subunit sequences remained unresolved. There was no clustering of subunits derived from the same array or the same chromosome (Figure 1B). Bayesian tree analysis produced one significantly supported cluster composed of 10 sequences derived from 7 chromosomes (Figure 1B).

TCAST transposon-like elements:

The second group of TCAST-like repeats is represented by a complex element that contains an almost complete TCAST (or Tcast1b) monomer, and a TCAST monomer segment of approximately 121 bp in an inverted orientation. These two TCAST segments are separated by a nonsatellite sequence of approximately 306 bp. Both TCAST segments are part of TIRs that are approximately 269 bp long (Figure 2). As a result of the long TIRs, these elements are likely to form stable hairpin secondary structures and therefore resemble transposons. The nonsatellite part of sequence, common for all TCAST transposon-like elements, is unique in that it does not exhibit significant homology to any other sequence within the T. castaneum genome. There were 34 TCAST transposon-like elements found within or in the vicinity of 50 genes. Their lengths (Table 1) and exact start and end sites within genomic sequence (Table S1) are provided. Sequence analysis of TCAST transposon-like elements determined that 13 of them were > 1000 bp, with a maximal size of 1181 bp (Table 1). The remaining TCAST transposon-like elements were shorter, with a minimal size of 314 bp (sequence no. 27), and usually lacking part of, or one or both, TIRs. Conserved TIRs are necessary for transposition, and if they are absent, truncated, or mutated so that the transposase cannot interact with the transposon sequence, the transposon cannot be mobilized and therefore represents a molecular fossil of a once active transposon (Capy et al. 1998). Despite mutations and partial truncations of TIRs within the TCAST transposon-like elements, and likely because of the length of the TIRs, most of the elements still preserve a stable secondary structure and could potentially remain mobile.

Figure 2 .

Figure 2 

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Organization of TCAST elements within T. castaneum genome in the form of TCAST transposon-like element, tandem arrays, and CR1-3_TCa retrotransposon. Regions corresponding to TCAST element are shown in red. TCAST transposon-like element contains an almost complete TCAST monomer and a monomer segment of approximately 121 bp in an inverted orientation, whereas CR1-3 retrotransposon contains segment corresponding to 1.2 monomer. Within TCAST transposon-like element terminal inverted repeats (arrows) unique nonsatellite sequence (green), target-site duplication in the form of “ACT,” and the insertion point of 925-bp sequence found within TR 1.9, element and coding for the putative transposase are shown. Three short ORFs within TCAST transposon-like element are also indicated. Within nonlong terminal repeat retrotransposon CR1-3_TCa regions corresponding to 5′UTR and to two ORFs are indicated.

Some TCAST transposon-like elements >1000 bp have a 3-bp duplication at the site of insertion in the form of ACT. One TCAST transposon-like element (sequence no. 39) is inserted into another repetitive DNA, indicated as Tcast2, which had been previously identified bioinformatically (Wang et al. 2008). Sequence analysis of this transposon-like element confirms the continuity of Tcast2 from the duplication site “ACT.” Typically, the size of target-site duplication is a hallmark of different superfamilies of eukaryotic DNA transposons, with mariner/Tc1, the only superfamily whose members are characterized by either 2- or 3-bp target-site duplication (Capy et al. 1998; Kapitonov and Jurka 2003; Feschotte and Pritham 2007). There are three open reading frames (ORFs) within TCAST transposon-like sequences, but the resulting putative proteins are very short and do not share similarity with any other proteins (Figure 2). The elements therefore do not code for transposases and are considered nonautonomous. Using the whole TCAST transposon-like elements as a query sequence, we searched the T. castaneum Gen Bank database for “full-sized” homologous elements that could potentially code for transposases and be considered autonomous. The search identified an element, named TR 1.9, with a 925-bp sequence inserted within a unique sequence of the TCAST transposon-like elements (Figure 2). This 925-bp sequence contains an ORF of 206 amino acids and a conserved domain belonging to the Transposase 1 superfamily, which also includes the mariner transposase. DNA transposons of the mariner/Tc1 superfamily Mariner-1_TCa and Mariner-2_TCa, were identified within the T. castaneum genome (Jurka 2009a, 2009b). Using BLASTP and the translated sequence from the 925 bp ORF as a query sequence, we identified hits with a partial homology to a Mariner-2_TCa transposase and to a mariner-like element transposase present in two other insects, the beetle Agrilus planipennis (emerald ash borer) and Chrysoperla plorabunda (green lacewing; Neuroptera), but not to Mariner-1_ TCa transposase.

To test whether there is any chromosome-specific sequence clustering of TCAST transposon-like sequences that could suggest difference in homogenization within chromosome and among different chromosomes, the alignment and subsequent phylogenetic analysis of TCAST transposon-like sequences was performed. Because TCAST transposon-like elements differ significantly in size (314−1181 nt), the alignment and phylogenetic analyses was performed on 25 elements that mutually overlap in their sequences, whereas the other nine TCAST transposon-like elements were excluded from the analysis due to the very low overlapping with other elements. Alignment was additionally adjusted using Gblocks (File S3). The average pairwise divergence among TCAST transposon-like sequences was 12.7%. ML and Bayesian methods gave similar tree topologies (Figure 1C). The ML tree showed very weak resolution of TCAST transposon-like sequences and a general absence of subgroups with specific sequence characteristics (Figure 1C). Only two clusters were formed whereas, using the Bayesian tree, we identified three well-supported groups; two of them were as for ML tree (Figure 1C).

Distribution of TCAST-like elements on T. castaneum chromosomes

TCAST-like elements found in the vicinity of genes were distributed on all 10 T. castaneum chromosomes (Table 1). Positions of constitutive heterochromatin and euchromatin were assigned on the haploid set of T. castaneum chromosomes, based on C-banding data (Stuart and Mocelin 1995) and Tribolium castaneum 3.0 Assembly data (Figure 3). Within euchromatic segments, the position of each TCAST-like element is specifically indicated (Figure 3) based on the position within the genomic sequence (Table S1). TCAST-like elements were dispersed on both arms of chromosomes 3, 5, 9, and 7, whereas on other chromosomes they were located on a single arm (Figure 3). The number of TCAST-like elements ranged from 2 on chromosome 1(X) to 17 on chromosomes 3 and 9. To detect whether TCAST-like elements were distributed randomly among the T. castaneum chromosomes or whether there was a significant over or underrepresentation of the elements on some chromosomes we performed hypergeometric distribution analysis test. The analysis revealed no statistically significant deviation in the number of TCAST-like elements among the chromosomes (Figure S1), pointing to their random distribution.

Figure 3 .

Figure 3 

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Distribution of TCAST-like elements on T. castaneum chromosomes. The karyotype representing the haploid set of T. castaneum chromosomes, and positions of constitutive heterochromatin (dark) and euchromatin (white) are depicted based on C-banding data (Stuart and Mocelin 1995) and T. castaneum 3.0 assembly (http://www.beetlebase.org). TCAST transposon-like elements (blue) and TCAST satellite-like elements (red) are shown. Two TCAST-like elements are represented as separate lines if they are at least 100 kb distant from each other.

To determine whether there was a target preference for the insertion of TCAST-like elements, for example high AT content or another sequence characteristic, we analyzed the AT content within 100 bp of the flanking regions for each TCAST -like element, from both 5′ and 3′ sites (Figure S2 and Figure S3). The average AT content of the flanking regions for both TCAST satellite-like elements and TCAST transposon-like elements did not differ significantly from the average AT content of the whole T. castaneum genome or from the AT content of randomly selected intergenic regions and introns. Thus, this finding suggests that with regard to AT content, there is no target preference for the insertion of TCAST-like elements. Furthermore, alignment and comparison of all flanking sequences of TCAST-like elements did not identify any common sequence motifs.

Genes in the vicinity of TCAST-like elements

Uniprot gene numbers were used as identifiers of genes located in the vicinity of TCAST-like elements (gene names shown in Table 1). Uniprot gene numbers for homologous genes found in Drosophila melanogaster are also indicated (Table 1). Detailed description of the genes, including molecular function of their protein products, biological processes in which these proteins are involved, and their cellular localization (cellular component), are shown (Table S1). Each identified gene is assigned to a particular TCAST-like element within its vicinity, and the precise position of TCAST-like elements in genomic sequence (start and end site) is indicated (Table S1). Functional analysis revealed that 17 of 101 genes correspond to putative uncharacterized proteins, whereas the remaining genes are involved in different molecular functions and diverse biological processes. Among the proteins, a proportion is characterized by ATP binding activity (13 proteins) and involvement in protein phosphorylation and /or signal transduction (9 proteins; Table S1).

To determine whether TCAST-like elements are distributed randomly relative to genes or whether they are overrepresented near specific groups of genes, we used GeneCodis 2.0 to provide a statistical representation of the genes associated with TCAST-like elements. Because many genes are still not annotated in T. castaneum and furthermore T. castaneum genomic data are not included in GeneCodis, we used gene numbers for orthologous genes from D. melanogaster for the analysis and compared them with the whole set of 14,869 genes annotated in D. melanogaster. Genecodis analysis revealed that TCAST-like elements are located near nine genes characterized as members of the immunoglobulin protein superfamily. Because there are only 134 immunoglobulin-like genes present within the total set of D. melanogaster genes, random distribution of TCAST-like elements would result in their occurrence near approximately a single immunoglobulin-like gene. The presence of TCAST-like elements in the vicinity of nine immunoglobulin-like genes therefore represents a statistically significant overrepresentation (0.00000427). All nine genes exhibit structural features of immunoglobulin-like, immunoglobulin subtype 1 and immunoglobulin subtype 2 proteins and are associated with the following TCAST transposon-like elements: 25 at the 3′end, 28 and 39 at the 5′ end, 32 and 40 within introns, and TCAST satellite-like elements: 8 at the 3′ end, 19 and 62 at the 5′ end, and 41 within intron (Table 1). A minimal distance between TCAST-like element and immunoglobulin-like gene was 7165 bp and a maximal 173,881 bp (Table 1). Molecular function of most of immunoglobulin-like genes is unknown, and they are involved in different biological processes such as cell adhesion, protein phosphorylation, and axon guidance (Table S1). Although all nine genes belong to immunoglobulin superfamily, they did not exhibit sequence similarity, which could suggest role of duplication in their evolution and spreading. The position of TCAST-like elements relative to the genes also was not consistent with the possibility that TCAST-like elements duplicated along with the immunoglobulin- like genes.

Overrepresentation of TCAST-like elements was also found near genes that exhibit ATP-binding activity and axon guidance properties but with a marginal significance (0.0183374 and 0.00865139). For the rest of genes, no significant overrepresentation of TCAST-like elements was detected. Thus, enrichment of TCAST-like elements in the vicinity of immunoglobulin-like genes potentially implicates a role of TCAST-like elements in the regulation of these genes.

Discussion

TEs are classified in several dozen families based on transposition mechanisms and different dynamics properties (Hua-Van et al. 2005). Active TEs encode the enzymes necessary for their transposition, either to move between nonhomologous regions in the genome or to copy themselves to other positions. In many cases, TEs do not produce their own enzymes but are able to use those from functional copies or even from other TEs families. Defective and inactive TEs often are amplified in regions of low recombination such as heterochromatin and may form tandemly repeated satellite DNAs. The origin of satellite DNA array from transposon-like elements is reported for many insects such as Drosophila melanogaster (Agudo et al. 1999), Drosophila guanche (Miller et al. 2000), and the beetle Misolampus goudoti (Pons 2004) whereas the retroviral-like features were first observed in the satellite DNA from rodents of the genus Ctenomys (Rossi et al. 1993).

Transposons can be inserted into other repetitive sequences such as satellite DNAs, as has been observed for the mariner-like element and MITE element, both inserted into satellite DNA of the ant Messor bouvieri (Palomeque et al. 2006). Searching for repetitive elements homologous to the TCAST repeat within Repbase (http://www.girinst.org/repbase/) revealed that 5′ UTR of nonlong terminal repeat retrotransposon CR1-3_TCa (Jurka 2009c) shares a high similarity of 83% with a 444-bp long TCAST sequence composed of 1.2 tandem monomers (Figure 1). Other CR1 subfamilies identified within T. castaneum such as CR1-1_ TCa, CR1-2_TCa, and CR1-4_TCa, published in Repbase, do not share similarity to CR1-3 and do not contain TCAST similar sequence. We propose that CR1-3 was inserted within TCAST satellite array and through recombination has acquired a part of TCAST sequence. Newly acquired TCAST element could act as a promoter because TCAST satellite DNA has an internal promoter for RNA Pol II (Pezer and Ugarković 2012) and becomes a new functional 5′ UTR. Subsequent retrotransposition of CR1-3_TCa could explain the dispersion of TCAST within the euchromatin (Figure 4). Three CR1-3_TCa elements with TCAST in the 5′UTR were identified within scaffolds that have not been mapped to linkage groups. However, truncated fragments with partial homology to CR1-3_TCa retrotransposon can be mapped within T. castaneum genome, some of them in the vicinity of TCAST elements. Such arrangement also indicates the role of CR1-3_TCa in the spreading of TCAST elements. There is also a possibility that TCAST satellite DNA originates from CR1-3 retrotransposon which was, after inactivation, amplified within the heterochromatin region. In the case of TCAST transposon-like elements, part of the satellite sequence is incorporated within TIRs which are characteristic for DNA transposons. The presence of target-site duplications at the sites of insertions of some TCAST transposon-like elements also indicates transposition as a mode of spreading of TCAST elements. Parts of satellite DNA elements can be found within some transposons, such as pDv transposon (Evgen'ev et al. 1982; Zelentsova et al. 1986) whose long direct terminal repeats show significant sequence similarity to the pvB370 satellite DNA, located in the centromeric heterochromatin of a number of species of the Drosophila virilis group (Heikkinen et al. 1995). The presence of short stretches of PisTR-A satellite DNA sequences within 3′ UTR of Ogre retrotransposons dispersed in the pea (Pisum sativum) genome was reported (Macas et al. 2009). Furthermore, the mobilization of subtelomeric repeats upon excision of the transposable P element from tandemly repeated subtelomeric sequences has been observed (Thompson-Stewart et al. 1994).

Figure 4 .

Figure 4 

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Models of spreading of TCAT-like elements based on (A) retrotransposition of CR-3_TCa element. CR1-3_TCa was inserted within TCAST satellite array and through recombination has acquired a part of TCAST sequence, which could act as a promoter and become a new functional 5′UTR. Subsequent retrotransposition of CR1-3_TCa could explain the dispersion of TCAST within the euchromatin. (B) Rolling circle replication of TCAST satellite DNA sequences excised from their heterochromatin loci via intrastrand recombination, followed by reintegration into different genome locations by homologous recombination.

Incorporation of part of a TCAST satellite DNA sequence into a (retro)transposable element, and its subsequent mobilization and spreading by (retro)transposition, may explain the distribution of TCAST element in the vicinity of genes within euchromatin. Satellite DNA sequences are prone to undergo recurrent repeat copy number expansion and contraction in divergent lineages as well as among populations of the same species (Bosco et al. 2007). This amplification appears to be random and does not correlate with phylogeny of the species (Pons et al. 2004; Lee et al. 2005; Bulazel et al. 2007). Amplification of a satellite sequence is reported to occur as a result of unequal crossing over or duplicative transposition (Smith 1976; Ma and Jackson 2006). The discovery of human extrachromosomal elements originating from satellite DNA arrays in cultured human cells and different plant species indicates the possible existence of additional amplification mechanisms based on rolling-circle replication (Assum et al. 1993; Navrátilová et al. 2008). It has been proposed that satellite sequences excised from their chromosomal loci via intrastrand recombination could be amplified in this way, followed by reintegration of tandem arrays into the genome (Feliciello et al. 2006). Moreover, it is possible that such a mechanism affected TCAST satellite DNA, and that extrachromosamal circles of TCAST were reintegrated into different genome locations by homologous recombination based on short stretches of sequence similarity between TCAST satellite and target genomic sequence (Figure 4). Integrated TCAST sequences are mainly composed of interspersed elements belonging to two major subfamilies, Tcast1a and Tcast1b, which is a prevalent type of organization in pericentromeric heterochromatin (Feliciello et al. 2011). This finding indicates that the origin of dispersed euchromatic TCAST elements may be duplication of heterochromatin copies.

The distribution of TCAST-like elements relative to protein coding genes revealed no specific preference for insertions within introns or at 5′ or 3′ ends of genes. TCAST-like elements are distributed on all chromosomes with no significant deviation in the number among the chromosomes, and phylogenetic analysis did not detect any significant sequence clustering of TCAST-like elements derived from the same chromosome. Dispersed TCAST satellite-like elements produce tandem arrays up to tetramers, but repeats from the same array do not reveal any significant clustering on phylogenetic trees. This finding indicates there is no significant difference in the homogenization of TCAST satellite-like repeats at the level of local arrays or chromosome or among different chromosomes. The average pair-wise sequence divergence (6% for dispersed TCAST satellite-like repeats) is greater than the usual divergence of satellite elements located in heterochromatin of tenebrionid beetles [approximately 2% (Ugarković et al. 1996)]. This difference in homogeneity between repeats located in heterochromatin and euchromatin may be explained by a lower rate of gene conversion affecting dispersed satellite-like elements or by a specific mechanism of DNA repair acting on satellite DNA (Feliciello et al. 2006). TCAST transposon-like elements dispersed among the genes within euchromatin have an even greater average sequence divergence (approximately 12%) and also exhibit no significant chromosome-specific sequence clustering, indicating a similar rate of homogenization within and among the chromosomes. Relatively high sequence divergence of TCAST transposon-like elements and the significant truncation of the majority of them, indicates that the transposition of these elements did not occur very recently and that these elements could be considered as molecular fossils of the functional TCAST transposon-like elements.

Cis-regulatory elements, such as promoters or transcription factor binding sites, are predicted in some satellite DNAs (Pezer et al. 2011). Transcription from promoters for RNA Pol II is also characteristic for pericentromeric satellite DNAs from the beetles Palorus ratzeburgii and Palorus subdepressus (Pezer and Ugarković 2008, 2009). Temperature-sensitive transcription of TCAST satellite DNA from an internal RNA Pol II promoter has been demonstrated (Pezer and Ugarković 2012). Based on these findings, it can be proposed that TCAST elements located in the vicinity of genes may function as alternative promoters, and transcripts derived from them may interfere with the expression of neighboring gene. This type of regulation is often observed for retrotransposons positioned immediately 5′ of protein genes (Faulkner et al. 2009). In addition, some tissue-specific gene promoters are derived from retrotransposons (Ting et al. 1992; Samuelson et al. 1996). Because of rapid evolutionary turnover, satellite DNA sequences often are restricted to a group of closely related species, or in some instances are species specific. This is the case with TCAST satellite DNA, which is not even detected in the congeneric Tribolium species. If restricted satellite DNAs have regulatory potential, then insertion of these elements in vicinity of genes could contribute to the establishment of lineage-specific or species-specific patterns of gene expression. Annotation of genes in proximity to TCAST-like elements demonstrated a statistical overrepresentation of certain groups of genes, for example, those with immunoglobulin-like domains. Recently, in the fish Salvelinus fontinalis, a regulatory role of a 32-bp satellite repeat, located in an intron of the major histocompatibility complex gene (MHIIβ), on MHIIβ gene expression was demonstrated (Croisetiere et al. 2010). The level of gene expression depends on temperature, as well as the number of satellite repeats, and indicates a role for temperature-sensitive satellite DNA in gene regulation of the adaptive immune response. Further studies are necessary to determine whether TCAST-like elements exhibit a potential regulatory role on nearby genes. The transcriptional potential of satellite DNAs as well as their distribution close to protein-coding genes, as shown in this study, provides strong support, that in addition to transposons, satellite DNAs represent a rich source for the assembly of gene regulatory systems.

Supplementary Material

Supporting Information
supp_2_8_931__index.html (2.2KB, html)

Acknowledgments

This work was supported by Croatian Ministry of Science, Education and Sport (grant no. 098-0982913-2832), European Union FP6 Marie Curie Transfer of Knowledge (grant MTKD-CT-2006-042248), and COST Action TD0905 “Epigenetics: Bench to Bedside.”

Footnotes

Communicating editor: J. A. Scott

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supp_2_8_931__index.html (2.2KB, html)
supp_2.8.931_003467SI.pdf (450.3KB, pdf)
supp_2.8.931_FigureS1.pdf (178.3KB, pdf)
supp_2.8.931_FigureS2.pdf (134.3KB, pdf)
supp_2.8.931_FigureS3.pdf (125.2KB, pdf)
supp_2.8.931_TableS1.pdf (170.2KB, pdf)
supp_2.8.931_FileS1.ppt (1MB, ppt)
supp_2.8.931_FileS2.ppt (1.2MB, ppt)
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