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Frontiers of Agricultural Science and Engineering

ISSN 2095-7505

ISSN 2095-977X(Online)

CN 10-1204/S

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Front. Agr. Sci. Eng.    2017, Vol. 4 Issue (4) : 421-432    https://doi.org/10.15302/J-FASE-2017160
RESEARCH ARTICLE
Repeats in the transcribed regions: comprehensive characterization and comparison of Citrus spp.
Manosh Kumar BISWAS1, Christoph MAYER2, Xiuxin DENG1()
1. Key Laboratory of Horticultural Plant Biology, Ministry of Education/Huazhong Agricultural University, Wuhan 430070, China
2. Center of Molecular Biodiversity, Forschungsmuseum Alexander Koenig, Adenauerallee, Bonn 53113, Germany
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Abstract

A large number of expressed sequences tags are available for Citrus spp., which provides an opportunity to understand genomic organization of the transcribed regions. Here, we report a detailed analysis of repetitive elements including tandem repeats (TRs) and transposable elements (TEs) in the transcribed region of the Citrus spp. On average, 22% of the expressed sequence tags (ESTs) contain TRs. The relative density of TR classes is highly taxon-specific. For instance, Citrus limonia has a high relative density of mononucleotide repeats, whereas dinucleotide repeats are rare. The proportions of 2–6, 7–30 and 31–50 bp repeats were almost identical in all studied species except for C. limonia and C. limettioides. We found that<1% of the citrus ESTs have a similarity with transposable elements. Transcriptional activity of transposable element families varied even within the same class of elements. A high proportion of transcriptional activity was observed for gypsy-like TEs compare to other TE classes. While TEs are relatively rare, TRs are abundant elements in ESTs of citrus. The high proportion of TRs that have a unit size longer than 6 bp raises the question about a possible functional or evolutionary role of these elements.
Keywords Citrus spp.      tandem repeats      transcribed region      transposable elements     
Corresponding Author(s): Xiuxin DENG   
Just Accepted Date: 10 May 2017   Online First Date: 26 May 2017    Issue Date: 10 December 2017
 Cite this article:   
Manosh Kumar BISWAS,Christoph MAYER,Xiuxin DENG. Repeats in the transcribed regions: comprehensive characterization and comparison of Citrus spp.[J]. Front. Agr. Sci. Eng. , 2017, 4(4): 421-432.
 URL:  
https://academic.hep.com.cn/fase/EN/10.15302/J-FASE-2017160
https://academic.hep.com.cn/fase/EN/Y2017/V4/I4/421
Species No. of sequences
analyzed*		 Total length of sequences/bp CG content/% No. of TR containing EST/% No. of TE containing
EST/%		 TR frequency
(TR/Mbp)		 TE frequency
(TE/Mbp)		 TR coverage/%
Citrus sinensis 70917 63428301 45.24 16153 (22.78) 1819 (2.56) 2439 29 6.89
Citrus clementina 24201 22433389 44.62 4930 (20.37) 546 (2.26) 2299 24 5.98
Citrus trifoliata 25388 22799411 46.47 6107 (24.05) 262 (1.03) 2646 11 7.86
Citrus reticulata 29422 26697646 47.51 6736 (22.89) 188 (0.64) 2410 7 6.91
Citrus unshiu 8328 4826095 41.92 861 (10.34) 77 (0.92) 1802 16 4.48
Citrus auruntium 10260 8244717 47.97 2112 (20.58) 30 (0.29) 2469 4 6.90
Citrus limonia 7895 6627791 44.80 1943 (24.61) 60 (0.76) 3030 9 8.32
Citrus latifolia 7173 6313905 48.56 1635 (22.79) 53 (0.74) 2488 8 6.69
Citrus aurantifolia 5977 5093917 49.46 1574 (26.33) 13 (0.22) 3003 3 8.64
Citrus limettioides 7049 6393162 44.62 2257 (32.02) 18 (0.26) 3401 3 9.05
Citrus paradisi 4358 2549165 41.78 385 (8.83) 17 (0.39) 1608 7 4.48
Total 200968 175407499 45.72 44693 (22.24) 3083 (1.53) 2488 18 6.93 ?
Tab.1  List of Citrus spp. and the number of sequences analyzed in the present study together with basic characteristics of these sequences
Fig.1  Density and length characteristics of tandem repeats (TRs) in the transcribed regions of 11 Citrus spp. (a) TR density versus size of the expressed sequence tag (EST) data set; (b) mean repeat length versus size of the EST data set; (c) relative frequency of TR classes.
Species Microsatellite (1–6 bp) Minisatellite (7–100 bp) Satellite (>100)
NL ANRL Var. Den. Cov. NL ANRL Var. Den. Cov. NL ANRL Var. Den. Cov.
Citrus sinensis 1164 13 502 26611 2.66 1271 3 31609 40558 4.06 4 3 246 1707 0.17
C. clementina 1254 10 484 25738 2.57 1039 3 11414 31960 3.20 5 3 94 2079 0.21
C. trifoliata 1242 14 485 30582 3.06 1396 3 15612 45889 4.59 5 3 101 2120 0.21
C. reticulata 1076 10 491 23002 2.30 1327 3 17248 44461 4.45 3 3 91 1602 0.16
C. unshiu 956 7 405 18391 1.84 840 2 2873 24257 2.43 6 2 29 2134 0.21
C. auruntium 1086 9 457 22786 2.28 1379 3 6865 42890 4.29 6 3 51 3282 0.33
C. limonia 1550 17 394 36353 3.64 1474 3 4942 44002 4.40 6 3 41 2858 0.29
C. latifolia 1073 11 406 22791 2.28 1414 3 5245 42758 4.28 3 2 20 1359 0.14
C. aurantifolia 1291 11 410 29151 2.92 1703 3 5178 55022 5.50 5 3 24 2189 0.22
C. limettioides 1690 14 399 35493 3.55 1710 3 5325 53125 5.31 4 3 24 1873 0.19
C. paradise 866 6 338 5720 1.64 736 2 1511 7413 2.10 7 3 18 1703 0.32
Over all 2.65 4.12 0.19
Tab.2  Summary statistics of the tandem repeat in the transcribed regions of 11 citrus genomes
Repeat type C. sinensis C. clementina C. trifoliata C. reticulata C. unshiu C. auruntium C. limonia C. latifolia C. aurantifolia C. limettioides C. paradisi Min Max
A 197.1 175.1 217.2 112.4 83.9 101.4 500.3 157.3 130.2 481.9 55.3 55.3 500.3
C 82.1 89.2 99.3 96.7 3.3 78.1 230.8 70.3 107.6 248.4 4.7 3.3 248.4
AC 4.7 5.5 4.4 3.6 6.0 3.9 2.9 3.3 3.1 1.3 7.1 1.3 7.1
AG 17.7 28.1 16.4 17.6 27.1 14.4 7.4 11.4 16.3 13.6 24.7 7.4 28.1
AT 9.4 9.2 9.5 7.5 13.9 6.5 8.0 6.5 11.2 4.1 14.5 4.1 14.5
CG 0.4 0.1 0.4 0.3 0.0 0.7 0.0 0.2 1.0 0.0 0.0 0.0 1.0
AAC 3.2 6.2 3.6 3.0 4.1 3.0 1.7 1.9 4.5 0.8 4.7 0.8 6.2
AAG 12.2 17.3 11.4 11.3 14.9 10.9 8.8 8.4 10.0 8.9 14.5 8.4 17.3
AAT 9.6 12.4 8.2 7.0 11.8 7.4 5.4 4.1 6.7 4.5 14.5 4.1 14.5
ACC 3.4 7.4 3.5 2.9 2.7 3.5 0.6 2.9 3.7 2.7 4.3 0.6 7.4
ACG 1.2 3.2 1.7 0.9 2.3 1.0 0.6 0.5 1.2 1.1 0.8 0.5 3.2
ACT 0.4 1.1 0.6 0.3 0.6 0.4 0.3 1.0 0.6 0.2 1.6 0.2 1.6
AGC 8.0 11.5 6.9 8.5 6.8 10.2 3.8 7.3 8.2 6.1 11.4 3.8 11.5
AGG 3.5 6.9 3.0 4.5 5.2 3.2 0.8 1.4 2.9 3.4 2.4 0.8 6.9
ATC 5.1 8.2 5.0 4.2 7.5 3.8 4.8 2.1 5.7 3.6 8.2 2.1 8.2
CCG 2.2 7.0 3.4 2.7 3.3 2.9 1.5 2.1 1.6 1.1 3.1 1.1 7.0
Tab.3  Density (TRs/Mbp) of different TR types from mono- to tri-nucleotides repeats for EST data sets of all 11 Citrus spp.
Fig.2  Comparative features of the distribution of TRs in the transcribed regions of 11 citrus species. (a) Number of Tandem Repeats (TRs) per Mbp; (b) number of different units found per Mbp genome; (c) average no of repeat units per locus; (d) genomic density of TRs in the three different unit size ranges 1–6 bp, 7–10 bp and 11–50 bp for 11 Citrus spp.
Fig.3  (a) Number of expressed sequence tags (ESTs) similar to transposable element (TE) families for 11 Citrus spp.; (b) number of ESTs similar to TE families in the collection of all ESTs from 11 Citrus spp.; (c) percentage distribution of EST among major class of TEs; (d) dot-plot correlation between TE copy number and number of EST similar to the TE.
Fig.4  Phylogenetic analysis of long-terminal repeat-retrotransposon sequences in citrus expressed sequence tag and genomic sequences. (a) Phylogenetic tree based on copia-like sequences; (b) phylogenetic tree based on gypsy-like sequences.
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