Skip to main content
NCBI home page
PLOS One logoLink to PLOS One
. 2021 Nov 11;16(11):e0259540. doi: 10.1371/journal.pone.0259540

CicerSpTEdb: A web-based database for high-resolution genome-wide identification of transposable elements in Cicer species

Morad M Mokhtar 1,*, Alsamman M Alsamman 1, Haytham M Abd-Elhalim 2, Achraf El Allali 1,*
Editor: Khalil Kashkush3
PMCID: PMC8584679  PMID: 34762703

Abstract

Recently, Cicer species have experienced increased research interest due to their economic importance, especially in genetics, genomics, and crop improvement. The Cicer arietinum, Cicer reticulatum, and Cicer echinospermum genomes have been sequenced and provide valuable resources for trait improvement. Since the publication of the chickpea draft genome, progress has been made in genome assembly, functional annotation, and identification of polymorphic markers. However, work is still needed to identify transposable elements (TEs) and make them available for researchers. In this paper, we present CicerSpTEdb, a comprehensive TE database for Cicer species that aims to improve our understanding of the organization and structural variations of the chickpea genome. Using structure and homology-based methods, 3942 C. echinospermum, 3579 C. reticulatum, and 2240 C. arietinum TEs were identified. Comparisons between Cicer species indicate that C. echinospermum has the highest number of LTR-RT and hAT TEs. C. reticulatum has more Mutator, PIF Harbinger, Tc1 Mariner, and CACTA TEs, while C. arietinum has the highest number of Helitron. CicerSpTEdb enables users to search and visualize TEs by location and download their results. The database will provide a powerful resource that can assist in developing TE target markers for molecular breeding and answer related biological questions.

Database URL: http://cicersptedb.easyomics.org/index.php

Introduction

Transposable elements (TEs) are mobile DNA sequences that can move and integrate themselves in another location throughout the genome [1]. Based on the transposition systems, TEs were classified into two classes [2]. Class I is known as retrotransposons, and Class II is known as DNA transposons. Retrotransposons utilize a copy and paste system, while DNA transposons use the cut and paste systems to transpose along the genome [2]. Retrotransposons are divided into two sub-classes, the long terminal repeat-retrotransposons (LTR-RT) and the non-LTR retrotransposons [2]. More evidence documented that TEs contribute to the reshaping of plant genomes and play important roles in regulating, altering, and creating new genes, as well as its essential role in the evolutionary dynamics of host genomes [3–5]. Many reports discussed in detail the impacts of TEs in both the genome and the epigenome [6, 7], the creation of pseudo-gene [8], the alteration [8], and transcriptional silencing [9, 10]. Moreover, TEs affect the development of both vertebrates [11] and plants [12]. In rice, maize, wheat, and barley, there is a correlation between the insertion of TEs near genes and the increased mutation rates in regulatory regions and coding sequences [13]. TEs represent a large percentage of plant genomes, such as rice 40% [14], maize, and wheat 85% [15, 16]. In plants, researchers have found evidence that TEs affect agronomic traits for maize [17], grape [18], foxtail millet [19], blood oranges [20], apples [21, 22] and others. Since TEs play an important role in genome variations, their genetic variation could be considered advantageous for crop breeding [23–26].

The Cicer genus contains 45 species with nine annual and 36 perennial species. Only chickpea (Cicer arietinum L.) is cultivated in 49 countries on a large scale. Currently, only two annual Cicer species (Cicer reticulatum and Cicer echinospermum) are in the primary and secondary gene pools and crossable to chickpea [27]. Chickpea is one of the most important Fabaceae crops. It has special significance to food security in developing countries due to its potential nutritional and health benefits [28]. According to 2019 FAO statistics [29], about 13.7 million hectares were cultivated with chickpea in more than 47 countries, yielding about 14.2 million tons. As a member of the Fabaceae family, chickpeas can restore soil fertility by fixing atmospheric nitrogen [30]. Because of its value for the economy and human nutrition, chickpea-related research has also increased interest, especially in crop improvement, genetic, genomics, and basic biological studies [31].

A significant achievement in Cicer species genomics was attained as a result of publishing the genomic sequences of Cicer arietinum [30–32], Cicer reticulatum [33], and Cicer echinospermum [34]. Chickpea genomic studies aim to improve our knowledge of genome organization, structural variations, genome evolution, and the basic biology of legume crops. Advances in bioinformatics and sequencing technologies have led to the fast creation of large-scale sequencing and genotyping data sets for chickpea [35–37]. The integrated study of massive phenotypic and genomics data opens the door for discovering new genes, functional elements, and biological processes correlated with several economic traits [38].

The fast-growing of chickpea omics data led to the establishment of many functional genomics databases, including the microsatellites markers database "CicArMiSatDB" [39], the SNP and InDels database "CicArVarDB" [40], and the transcriptome database "CTDB" [41]. In recent years, functional genomic elements such as miRNAs [42], transcription factors [38], long non-coding RNAs [43], and transposable elements [44] were discovered for several plant species. For chickpea, miRNAs were identified in 2014 [45], transcription factor in 2016 [46], and long non-coding RNAs in 2017 [47].

At present, several multiple-species TE databases are available and are exemplified by Repbase [48], GyDB [49], PlantsDB [50], and RepetDB [51]. Species-specific TE databases are also available such as RetrOryza [52], BmTEdb [53], BrassicaTED [54], MnTEdb [55], FmTEMDb [56], PlanTE-MIR DB [57], SPTEdb [58], and ConTEdb [59]. Despite advancements in functional genome annotation of chickpea, no database for chickpea TEs has been established. Chickpea TEs need to be clearly identified in detail and made available to researchers. Studying these valuable genomic elements should accelerate the improvement of this important crop and become a new area of research in chickpea.

Genome-wide identification of TEs in the Cicer species and the establishment of comprehensive TE databases are key resources for the accurate characterization of genes and other genomic elements. Here, we used the Extensive de-novo TE Annotator (EDTA) pipeline [60] as both structure and homology-based methods to identify, classify and annotate TEs in Cicer species. All identified TEs were deposited for browsing and visualization in the developed Cicer species Transposable Elements database (CicerSpTEdb). CicerSpTEdb will represent an open resource that will allow researchers to improve our knowledge of the origin, organization, structural variations, and evolution of the Cicer species, including the chickpea genome. The CicerSpTEdb database will also provide an essential resource to other related legume crops. In addition, we hope that CicerSpTEdb aid plant breeders in developing TE target markers for molecular breeding and help the research community in general answer related biological questions.

Materials and methods

Genomic data

We retrieved the chickpea (C. arietinum) reference genome sequence of Kabuli type cultivar CDC-Frontier (ASM33114v1) from the NCBI FTP server [61] in both fasta and gff formats. Due to the unavailability of annotations, only fasta files were downloaded for Cicer reticulatum (GCA_002896235.1) and Cicer echinospermum (GCA_002896215.2) from NCBI FTP server [61].

Identification of TEs

We conducted the intact transposon identification and characterization for the 530, 657, and 715 Mbps representing the Cicer arietinum, Cicer echinospermum, and Cicer reticulatum reference genome, respectively, using EDTA pipeline [60]. EDTA pipeline combines tools for the structure, homology-based, and de novo identification methods. The EDTA pipeline combines LTRharvest [62], LTR_FINDER [63], LTR_retriever [64], Generic Repeat Finder [65], TIR-Learner [66], HelitronScanner [67], and RepeatModeler [68]. The parameters of each tool are described in S1 File.

Estimation of LTR-RT insertion time

ClustalW [69] was used to alignment the 5′and 3′ LTRs of each intact LTR-RTs to estimate the insertion time of LTR-RTs. The nucleotide substitutions/divergence among LTRs (K) were computed by applying the Kimura-2-parameter model [70] using the KaKs_Calculator program [71]. Using an evolutionary rate (r) of 1.5 × 10−8 substitutions per synonymous site per year [72–74] and the formula T = k/2r the insertion time was estimated [70].

Identification of TEs positioned inside or nearby genes

Perl scripts were used to differentiate the predicted TEs according to the localization in the genome sequence. The goal was to identify TEs that are positioned within or nearby genes according to the genome annotation. For nearby genes, 10 kbp upstream genes were used to detect TEs located inside this region. We performed gene ontology on all genes that house TEs using UniProtKB [75].

Protein-protein interaction analysis

The amino acid sequences of genes that contain or are close to TEs were used for protein-protein interaction analysis using the STRING database [76]. Cytoscape 3.8.2 software and the STRING-App were used for PPI networks analysis and visualization [77, 78].

Database construction

JBrowse [79] was embedded in our developed database to map and visualize identified TEs across the reference genome. The CicerSpTEdb database was designed as an interactive web application using CSS, Perl, MySQL, PHP, HTML, and JavaScript. (Fig 1) illustrates the framework used to identify TEs in Cicer species and develop the proposed CicerSpTEdb.

Fig 1. The overall framework used for identifying and characterizing TEs in Cicer species and the steps involved in creating CicerSpTEdb.

Fig 1

Open in a new tab

Results and discussion

TEs identification and annotation have been formed for numerous plant genomes through extensive efforts and manual identification, e.g., Arabidopsis [80], rice [14], and maize [81]. Despite the increase in the number of sequenced plant genomes, manual identification remains labor-intensive, and automated TE annotation is needed [60]. Intact TEs are the complete structures of TEs that can transpose throughout the genome [82]. Most sequenced plant genomes have had annotated TEs. However, it is important to predict which of these TEs are still viable for mobility. Thus, in the present investigation, we focused only on the analysis of intact TEs. Using the EDTA pipeline [60], several approaches were applied to identify intact TEs in the C. arietinum, C. reticulatum, and C. echinospermum genomes. EDTA consist of LTRharvest [62] and LTR_FINDER [63] for LTR identification. False discoveries are filtered by LTR_retriever [64]. In addition, TIR-Learner [66] is used for TIR candidates identification, and HelitronScanner [67] is used to recognize Helitron candidates.

TEs identification in Cicer species

As a result, a total of 794 intact LTR-RTs were identified in C. arietinum, including 521 Copia, 80 Gypsy, and 193 unknown LTRs. For DNA TEs, we identified 775 Mutator followed by 245 CACTA, 215 hAT, 156 helitrons, 28 Tc1 Mariner, and 27 PIF Harbinger (Table 1). S1 Table includes details of the identified TEs, including the chromosome/scaffold id, TE start and end position in the genome, TE corresponding superfamily, and TE length.

Table 1. Summary of the intact TEs identified in Cicer species.

TE superfamily Cicer arietinum Cicer reticulatum Cicer echinospermum
No. elements Total length (bp) Percentage of the genome (%) No. elements Total length (bp) Percentage of the genome (%) No. elements Total length (bp) Percentage of the genome (%)
Copia 521 2692203 0.507 1097 7294492 1.02 1404 10055403 1.53
Gypsy 80 466654 0.088 267 1983455 0.277 423 3515110 0.535
Unknown LTR 193 578105 0.109 407 1514753 0.212 445 1766078 0.269
CACTA 245 594115 0.112 329 822381 0.115 291 757423 0.115
hAT 215 211394 0.04 211 231880 0.032 263 274877 0.042
Helitron 156 1498699 0.282 151 1142623 0.16 152 1438982 0.219
Mutator 775 1001091 0.189 1025 1397305 0.195 892 864817 0.132
PIF Harbinger 27 21975 0.004 56 100906 0.014 40 52275 0.008
Tc1 Mariner 28 40588 0.008 36 56626 0.008 32 43869 0.007
Total 2240 7104824 1.339 3579 14544421 2.033 3942 18768834 2.857
Open in a new tab

Interestingly, Varsheny et al. [30] reported that approximately 49.41% of the C. arietinum genome is composed of TEs and unclassified repeats, including 617,505 repeat retrotransposons and 197,959 DNA transposons. However, our investigation produced lower numbers and found that the intact TEs represent only 2240 elements, approximately 1.3% of the whole genome. This difference could be because many of them will not be intact TEs and may be nested elements or fragmented.

(Fig 2) shows the distribution and histogram of TEs across eight C. arietinum chromosomes. As shown, the distribution of TEs superfamily were 217, 179, 187, 200, 230, 240, 200, 76 elements for chromosomes 1, 2, 3, 4, 5, 6, 7, and 8, respectively. Chromosome 6 (CA6) had the highest presence of TEs (240 elements), including 57 Copia, 55 Mutator, 29 unknown, 27 CACTA, 27 hAT, 21 helitrons, 12 Gypsy, 9 PIF, and 3 Tc1_mariner.

Fig 2. The distribution of intact TEs across eight chickpea chromosomes.

Fig 2

Open in a new tab

The outermost circle in pink-colored represents eight C. arietinum chromosomes (CA1 to CA8). The middle circle illustrates the distribution of TE types in different colors, and the innermost circle shows the histogram of TE types in each chromosome.

The analysis of C. reticulatum TEs revealed that 14.54 Mb (approximately 2% of the genome) were intact TEs. The highest copy number of LTR-RT was 1097 Copia, followed by 193 unknown LTRs, and 80 Gypsy. In addition, 1808 C. reticulatum DNA transposons were detected and consist of 1025 Mutator, 329 CACTA, 211 hAT, 151 helitrons, 56 PIF Harbinger, and 36 Tc1 Mariner (Table 1 and S2 Table). For C. echinospermum, a total of 3942 intact TEs were detected and covered 18.76 Mb (approximately 2.8% of the genome). Out of these, 2272 LTR-RTs included 1404 Copia, 423 Gypsy, and 445 unknown LTRs. C. reticulatum has more Mutator, PIF Harbinger, Tc1 Mariner, and CACTA TE types (Table 1 and S3 Table). The present investigation revealed that C. reticulatum, C. echinospermum, and C. arietinum have a higher copy number of Copia superfamily than Gypsy, which is consistent with previous reports of flax [73], grape [83], cocoa [84], and cucumber [85].

To our knowledge, there are no TE reports for both C. echinospermum and C. reticulatum to allow the discussion of our new findings. In addition, the draft genomes of C. reticulatum, C. echinospermum, and C. arietinum were partially sequenced. The sizes of their available sequences are 530, 657, and 715 Mb, respectively. This variation in size could be correlated with the variation of the identified copy number of TEs in these genomes.

Estimation of LTR-RT insertion time

It is deemed that the 5′ and 3’ LTRs are the same at transposition time for each LTR-RT. Consequently, based on nucleotide substitutions/divergence among LTR-RT, the 5’ and 3’ LTRs accumulated through ages were applied to estimate the insertion time [86–88]. In the present investigation, the 5′ and 3’ LTR nucleotide substitutions were used to estimate the identified intact LTR-RT insertion time across Cicer species.

For C. arietinum, the minimum and maximum assumed age after discarding outliers using boxplot analysis ranged from 0 to 4.4 million years (MY) with an average of 0.94 MY. The unknown elements were older than Copia and Gypsy (4.3, 4.2, and 2.9 MY, respectively). The average insertion ages of the unknown, Copia and Gypsy elements are 1.3, 1.3, and 0.85 MY, respectively (Fig 3). Interestingly, about 23.3% of Copia, 21.7% of Gypsy, and 23.4% of unknown elements have estimated ages of < 0 MY, and they may still be active elements. While the proportions of insertion times that are more than 1.2 MY were 56.5%, 53.1%, and 40% of Gypsy, unknown, and Copia, respectively (Fig 3).

Fig 3. Estimation of Cicer species LTR-RT insertion age in millions of years (My).

Fig 3

Open in a new tab

For C. reticulatum, the estimated age ranged from 0 to 100 MY with an average of 33.7 MY. The unknown elements are younger than Copia and Gypsy elements. The Copia, Gypsy, and unknown elements’ average insertion times were 33.4, 40, and 28.7 MY, respectively. Overall, about 10.5% of Copia, 8.9% of Gypsy, and 7.5% of unknown elements were estimated to have an age of < 0 MY. While the proportions of insertion times that are more than 1.2 MY were 86%, 85.6%, and 81.9% of Gypsy, Copia, and unknown elements, respectively (Fig 3).

For C. echinospermum, the estimated age ranged from 0 to 99.5 MY with an average of 25.8 MY. The unknown elements are younger than Copia and Gypsy elements. The average insertion time of the Copia, Gypsy, and unknown elements were 30.3, 5.5, and 25.7 MY, respectively. Overall, about 6.6% of Gypsy, 12.5% of Copia, and 21.7% of unknown elements had an estimated age of < 0 MY. While the proportions of insertion times that are more than 1.2 MY were 87.5%, 78.7%, and 62.6% of Gypsy, Copia, and unknown elements, respectively (Fig 3).

The chromosomes number of the C. arietinum, C. echinospermum, and C. reticulatum were the same 2n = 16. Therefore C. reticulatum was in the primary gene pools and recognized as the wild ancestor of the C. arietinum. In addition, genetic studies revealed that the C. echinospermum was closely and in secondary gene pools of C. arietinum [27, 89]. The estimation of Cicer species LTR-RT insertion time revealed that the wild species C. echinospermum and C. reticulatum were older than the cultivated species C. arietinum (Fig 3). Based on estimated LTR-RT age, C. arietinum may be derived/split from their wild progenitor C. reticulatum ~ 4.4–6 MY.

TEs length distribution

The lengths of C. arietinum intact TEs ranged from 80 bp to 19.7 kb for both DNA and LTR transposons. The average sizes of various superfamilies were Gypsy 5.8 kb, Copia 5.1 kb, unknown LTR 2.9 kb, Helitron 9.6 kb, CACTA 2.4 kb, Tc1 Mariner 1.4 kb, Mutator 1.2 kb, hAT 0.9 kb, and PIF Harbinger 0.8 kb (Fig 4). For C. echinospermum TEs, lengths ranged from 80 bp to 19.6 kb for DNA and LTR transposons. The average sizes of various superfamilies were Gypsy 8.3 kb, Copia 7.1 kb, unknown LTR 3.9 kb, Helitron 9.4 kb, CACTA 2.6 kb, Tc1 Mariner 1.3 kb, PIF Harbinger 1.3 kb, hAT 1 kb, and Mutator 0.9 kb (S1 Fig). For C. reticulatum, TE lengths ranged from 80 bp to 21.7 kb for both DNA and LTR transposons. The average sizes of various superfamilies were Gypsy 7.4 kb, Copia 6.6 kb, unknown LTR 3.7 kb, Helitron 7.5 kb, CACTA 2.4 kb, PIF Harbinger 1.8 kb, Tc1 Mariner 1.5 kb, Mutator 1.3 kb, and hAT 1 kb (S2 Fig).

Fig 4. The distribution of C. arietinum TEs superfamilies according to their length.

Fig 4

Open in a new tab

Identification of TEs positioned inside or nearby genes

The transposition of TEs across the genome may affect both nearby genes’ expression and genes unlinked to the insertion. TEs can affect genes through the movement, duplication, and recombination processes, creating new genes or altering the gene structure [86]. Furthermore, they may alter the expression of nearby genes by inserting themself within cis-regulatory elements or by presenting a new cis-regulatory element that may act as gene enhancers or repressors [90]. Due to the unavailability of annotation for C. reticulatum and C. echinospermum, only TEs identified in C. arietinum were subject to further analysis to determine TEs that are inside or nearby genes.

Overall, 1162 C. arietinum intact TEs (about 51.8%) were positioned inside (TE-gene chimeras) or nearby genes. Only 20 TEs were found within pseudo-genes (Table 2). From these elements, 426 (approximately 36.6%) were LTR-RT, and 736 (approximately 63.3%) were DNA transposons. For LTR-RT, the Copia superfamily was overrepresented, followed by unknown elements and gypsy superfamilies with 250, 140, and 36 elements, respectively. However, DNA transposons included 326 Mutator, 173 hAT, 150 CACTA, 38 Helitron, 28 Tc1 Mariner, and 21 PIF Harbinger elements.

Table 2. Summary of the C. arietinum TEs that are positioned inside or nearby genes.

TEs superfamily Number of elements
Inside genes (TE-gene chimeras) Inside pseudo-genes Near genes (0-2kb) Near genes (2-10kb) Other genomic regions
Copia 100 5 29 116 271
Gypsy 27 1 1 7 44
Unknown LTR 91 2 3 44 53
CACTA 54 5 14 77 95
hAT 70 3 28 72 42
Helitron 9   10 19 118
Mutator 92 4 53 177 449
PIF Harbinger 9   1 11 6
Tc1 Mariner 19   1 8  
Total 471 20 140 531 1078
Open in a new tab

More evidence documented that TEs construct the chimeric genes (TE-gene chimeras) in plants [8, 91]. Previous eukaryotic reports revealed that one thousand human proteins contain TEs [92, 93], and few expressed genes house TEs in Drosophila [94]. In addition, approximately 1.2% of Arabidopsis proteins were constructed from TE-gene chimeras [95]. Consistent with our results, previous studies reported that Class I TEs favor transposition inside gene-poor heterochromatic regions [96]. In comparison, euchromatin regions have more Class II TEs that prefer to transposition inside or nearby genes [97–99]. The finding that TE elements inside and nearby genes in C. arietinum are overrepresented by Copia than Gypsy is consistent with previous studies in maize [100], Arabidopsis [95], and sugarcane [101].

Regarding class II TEs, Mutator was overrepresented, followed by hATs, while Helitrons were underrepresented. Our results agree with Lockton et al. [95] and Leonardo et al. [73], who found that hATs were overrepresented in Arabidopsis, while Helitrons were underrepresented in flax. Interestingly, the Mutator superfamily was overrepresented inside and closely to genes in C. arietinum. More evidence documented that the association between Mutator elements and genes supports TE-mediated gene transposition in rice [91] and Arabidopsis [102]. Finally, the distance between identified TEs near genes and genes ranged from 3 to 9.9 kb (S4 Table). From these TEs, 140 elements were located within 2kb near genes, among this 53 Mutator, 29 Copia, 28 hAT, 14 CACTA, ten Helitron, three Unknown_LTR, 1 Gypsy, 1 PIF_Harbinger, and 1 Tc1_Mariner.

Functional classification by gene ontology analyses

To determine whether the genes housing TEs in their sequence were disrupted or still have functions, UniProtKB [75] was used to map and classify 441 TE-gene chimeras according to their function (GO terms). Only 366 genes were successfully mapped to 482 UniProtKB IDs and assigned to GO terms. These GO terms include 315 genes assigned to 486 molecular functions GO terms (S3 Fig), 213 genes assigned to 393 biological processes GO terms (Fig 5), and 215 genes assigned to 325 cellular components GO terms (S4 Fig). The 393 GO terms assigned to biological processes were distributed among 164 cellular process, 134 metabolic process, 41 biological regulation, 29 response to the stimulus, 19 localization, two reproductive processes, two developmental processes, one flower development, and one response to another organism (Fig 5). Molecular function analysis showed the overrepresented TE-gene chimeras were catalytic activity, binding, and transporter activity. In contrast, the underrepresented TE-gene chimeras were DNA-binding transcription factor activity and Structural constituent of ribosome (S3 Fig). Based on these results, we can infer that a high percentage of TE-gene chimeras are still functional in various biological processes in C. arietinum. However, to determine their level of activity, further experimental validation still needs to be performed.

Fig 5. Gene ontology of 213 C. arietinum TE-gene chimeras assigned to 393 biological processes GO terms.

Fig 5

Open in a new tab

Protein-protein interaction analysis

Protein-protein interaction (PPI) analysis is an instrumental analysis tool. It can show how a group of genes interact in the cellular system and their activity level, thus showing their biological importance. Furthermore, it adds more information about the type of connection these proteins have and the biological pathways that they control. We examined the protein interaction activity of chickpea genes that contain or are close to TEs. The STRING database retrieved the interaction information of 619 proteins, from which high interactive proteins could be identified [76]. PPI analysis was carried out for genes that contain, or are close to, TEs, as well as for all genes collectively (Fig 6, S5 and S6 Figs).

Fig 6. Protein-protein interaction for TE-gene chimeras.

Fig 6

Open in a new tab

The most interactive gene was the DNA-directed RNA polymerase II subunit (RPB1), which contains nearby TEs (Fig 6). The RPB1 gene is an essential component of the RNA polymerase transcription machinery, catalyzing the transcription of DNA into RNA using the four ribonucleoside triphosphates as substrates [103]. Several research articles have discussed the relationship between RPB1 and TEs [104]. The carboxy-terminal domain of eukaryotic RPB1 has a heptad-repeat structure that is intrinsically disordered. These repeats regulate the length of the RPB1 C-terminal domain, which in turn controls transcription activation by influencing transcription cycle coordination. Such a relationship could impact the regulator’s system of essential cellular functions [105]. Phosphoglycerate kinase one gene (PGK1) also revealed many nearby TEs compared to other chickpea genes (S5 Fig). The activity of TEs influences polyploidization modifications in plant genomes, affecting the copy number and the content of genes. Due to its single-copy status per diploid chromosome in several plant species, the PGK1 gene has been widely used to reveal the evolutionary history of complex genomes [106, 107]. The String database offers the ability to analyze PPI networks depending on their biological pathways. It has revealed that the most gene-enriched pathways are those linked to Neclotide binding and metabolic pathways, and mostly, these genes are linked by lab experiments, published articles (text mining), or their genome physical distance (neighborhood) (S6 Fig). Out of these results, we can point out that TEs affect distinctive genes with high interplay activity and consequently impact a widespread biological process in the chickpea genome.

CicerSpTEdb web interface

The Cicer Transposable Elements database (CicerSpTEdb) is accessible through a user-friendly portal (http://cicersptedb.easyomics.org/index.php). The website allows users to explore and understand the Cicer transposable elements. The database offers comprehensive details of TEs and their features in the genome, especially for chickpea. The CicerSpTEdb interface allows users to search, browse, compare, and download TEs interactively. From the homepage, users can capture the essential information about CicerSpTEdb and access relative external databases and software. The navigation bar allows access to six sections for browsing and retrieving data, including Home, Database Search, JBrowse, Statistics, Comparisons, and Bulk Download.

The Database Search page

From anywhere on CicerSpTEdb’s interface, users can access the Database Search page through the top bar that links to the main search page. The latter provides links to access two separate Cicer arietinum pages. The first page allows a general search of TEs, while the second option provides detailed information on TEs located within genes. In addition, links to access Cicer reticulatum and Cicer echinospermum TE general search pages are also available. The top section of the TE general search page allows users to see a statistical chart of all identified TEs by type. The main section is divided into four sub-sections. It allows users to 1) search by TE type within a specific chromosome/scaffold or within the whole-genome, 2) search by TE type in a specific chromosome/scaffold or whole-genome with specific TE length, 3) search by TE type with a specific location inside the genome, 4) search by TE type with a specific length and location in the genome. The search results appear on a new page and include NCBI chromosome/scaffold accession, transposon start, end, length, and corresponding strand in the genome, TE structure details, download TE sequence, and a JBrowse link. The results can be exported by clicking the download button (Fig 7).

Fig 7. CicerSpTEdb’s TE general search page.

Fig 7

Open in a new tab

On the page dedicated to TEs located within genes, the left section is used to select TE types, and the top part of the page allows users to see a statistical chart of all identified TEs located inside genes. The main section is divided into four sub-sections that allow searching by different keys. Users can search using the gene ID and gene type (gene or pseudo-gene) or using either the protein ID, protein family, or enzyme EC number. The results are displayed on a separate page and include gene details (gene ID, symbol, location, type, and product), JBrowse link, and link to gene ontology and protein information. The link will redirect the user to a new page that contains all accessible protein information such as protein ID, names, length, structure, family, EC number, externally linked databases, and gene ontology. All external databases are cross-linked, and the results can be exported by clicking the download button (Fig 8).

Fig 8. CicerSpTEdb’s search page for TEs located within genes.

Fig 8

Open in a new tab

The JBrowse page

JBrowse is a powerfully interactive genome visualization tool established to illustrate the coordinates of TEs in the genome. By clicking the JBrowse from the top bar of any page, a visualization window will display all chickpea coordinates, including reference sequence, genes, and identified transposons. Users can retrieve any TE’s data (name, position in the genome, length, described information, and sequence) by clicking on it in the JBrowse graphic interface. In addition, the JBrowse page offers an important function that allows users to browse all genes around TEs and the genes that TEs are positioned inside. The latter visualization function is an easy way to build a clear idea of each TE and understand the interaction between TEs and the surrounding genes (Fig 9).

Fig 9. CicerSpTEdb’s JBrowse page.

Fig 9

Open in a new tab

Other pages

The Statistics page was created to provide researchers with a visualization of several statistics computed from the data in CicerSpTEdb. Users can access the Statistics page through a drop-down menu that links to three pages, one for each studied genome (S7 Fig). The comparisons page was created to provide researchers with a visual comparison of identified TEs between C. arietinum, C. reticulatum, and C. echinospermum. Users can access the comparison page through the top bar from any page (S8 Fig). The Bulk Download page was created to allow researchers to download all stored data in CicerSpTEdb. The Bulk Download page allows users to select the species, transposons, and data type (fasta or gff3 files) from organism name, TE type, and data type drop-down menus (S9 Fig).

Conclusion

CicerSpTEdb is the first comprehensive database designated to Cicer species transposable elements. This database contains 9761 TEs that combines DNA transposon and LTR retrotransposons. Moreover, the proposed database is available through an easy-to-use interface to allow researchers to search, browse, and download the identified TEs in C. echinospermum, C. reticulatum, and C. arietinum. We propose to continuously update the database and improve its applications to achieve its goals. We expect CicerSpTEdb to provide a valuable resource that can be used to improve our knowledge of the origin, organization, structural variations, and evolution of the Cicer species genomes and other related legume crops. CicerSpTEdb should help researchers develop TEs target markers for molecular breeding and to answer any related biological questions.

Supporting information

S1 Fig. The distribution of C. echinospermum TEs superfamilies according to their length.

(TIF)

Click here for additional data file. (990.2KB, tif)
S2 Fig. The distribution of C. reticulatum TEs superfamilies according to their length.

(TIF)

Click here for additional data file. (950.6KB, tif)
S3 Fig. Gene ontology of 315 C. arietinum TE-gene chimeras assigned to 486 molecular functions GO terms.

(TIF)

Click here for additional data file. (338.6KB, tif)
S4 Fig. Gene ontology of 215 C. arietinum TE-gene chimeras assigned to 325 cellular components GO terms.

(TIF)

Click here for additional data file. (537.3KB, tif)
S5 Fig. Protein-protein interaction for genes nearby TEs.

(TIF)

Click here for additional data file. (2.9MB, tif)
S6 Fig. Protein-protein interaction for both TE-gene chimeras and genes nearby TEs.

(TIF)

Click here for additional data file. (5.1MB, tif)
S7 Fig. CicerSpTEdb’s statistics page.

(TIF)

Click here for additional data file. (748.5KB, tif)
S8 Fig. CicerSpTEdb’s comparisons page.

(TIF)

Click here for additional data file. (895.2KB, tif)
S9 Fig. CicerSpTEdb’s bulk download page.

(TIF)

Click here for additional data file. (1.3MB, tif)
S1 Table. The details of the identified TEs in C. arietinum, including the chromosome/scaffold id, TE start and end position in the genome, TE corresponding superfamily, and TE length.

(XLSX)

Click here for additional data file. (97.2KB, xlsx)
S2 Table. The details of the identified TEs in C. reticulatum, including the chromosome/scaffold id, TE start and end position in the genome, TE corresponding superfamily, and TE length.

(XLSX)

Click here for additional data file. (161.4KB, xlsx)
S3 Table. The details of the identified TEs in C. echinospermum, including the chromosome/scaffold id, TE start and end position in the genome, TE corresponding superfamily, and TE length.

(XLSX)

Click here for additional data file. (165.9KB, xlsx)
S4 Table. The details of the identified TEs that located near genes in C. arietinum.

(XLSX)

Click here for additional data file. (68.1KB, xlsx)
S1 File. The programs and their parameters used for identification of TEs in Cicer species.

(DOCX)

Click here for additional data file. (23.5KB, docx)

Acknowledgments

The authors acknowledge the African Supercomputing Center at Mohamed VI Polytechnic University for the supercomputing resources (https://ascc.um6p.ma/) made available for conducting the research reported in this paper.

Availability

CicerSpTEdb is freely available at http://cicersptedb.easyomics.org/index.php

Data Availability

All relevant data are within the manuscript, Supporting Information files, and CicerSpTEdb is freely available at http://cicersptedb.easyomics.org/.

Funding Statement

The author(s) received no specific funding for this work.

References

  • 1.Finnegan DJ. Transposable elements in eukaryotes. Int Rev Cytol. Elsevier; 1985;93: 281–326. doi: 10.1016/s0074-7696(08)61376-5 [DOI] [PubMed] [Google Scholar]
  • 2.Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. Nature Publishing Group; 2007;8: 973–982. doi: 10.1038/nrg2165 [DOI] [PubMed] [Google Scholar]
  • 3.Bennetzen JL. Transposable element contributions to plant gene and genome evolution. Plant Mol Biol. Springer; 2000;42: 251–269. 10.1023/A:1006344508454 [DOI] [PubMed] [Google Scholar]
  • 4.Feschotte C. Transposable elements and the evolution of regulatory networks. Nat Rev Genet. Nature Publishing Group; 2008;9: 397–405. doi: 10.1038/nrg2337 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Bucher E, Reinders J, Mirouze M. Epigenetic control of transposon transcription and mobility in Arabidopsis. Curr Opin Plant Biol. Elsevier; 2012;15: 503–510. doi: 10.1016/j.pbi.2012.08.006 [DOI] [PubMed] [Google Scholar]
  • 6.Sahebi M, Hanafi MM, van Wijnen AJ, Rice D, Rafii MY, Azizi P, et al. Contribution of transposable elements in the plant’s genome. Gene. Elsevier; 2018;665: 155–166. doi: 10.1016/j.gene.2018.04.050 [DOI] [PubMed] [Google Scholar]
  • 7.Bennetzen JL, Wang H. The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu Rev Plant Biol. Annual Reviews; 2014;65: 505–530. doi: 10.1146/annurev-arplant-050213-035811 [DOI] [PubMed] [Google Scholar]
  • 8.Wang W, Zheng H, Fan C, Li J, Shi J, Cai Z, et al. High rate of chimeric gene origination by retroposition in plant genomes. Plant Cell. American Society of Plant Biologists; 2006;18: 1791–1802. doi: 10.1105/tpc.106.041905 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Lisch D. Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol. Annual Reviews; 2009;60: 43–66. doi: 10.1146/annurev.arplant.59.032607.092744 [DOI] [PubMed] [Google Scholar]
  • 10.Lin L, Tang H, Compton RO, Lemke C, Rainville LK, Wang X, et al. Comparative analysis of Gossypium and Vitis genomes indicates genome duplication specific to the Gossypium lineage. Genomics. Elsevier; 2011;97: 313–320. doi: 10.1016/j.ygeno.2011.02.007 [DOI] [PubMed] [Google Scholar]
  • 11.Yandım C, Karakülah G. Expression dynamics of repetitive DNA in early human embryonic development. BMC Genomics. 2019;20: 439. doi: 10.1186/s12864-019-5803-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Sun F, Guo W, Du J, Ni Z, Sun Q, Yao Y. Widespread, abundant, and diverse TE-associated siRNAs in developing wheat grain. Gene. Elsevier; 2013;522: 1–7. doi: 10.1016/j.gene.2013.03.101 [DOI] [PubMed] [Google Scholar]
  • 13.Wicker T, Yu Y, Haberer G, Mayer KFX, Marri PR, Rounsley S, et al. DNA transposon activity is associated with increased mutation rates in genes of rice and other grasses. Nat Commun. 2016;7: 12790. doi: 10.1038/ncomms12790 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Project IRGS. The map-based sequence of the rice genome. Nature. 2005;436: 793–800. doi: 10.1038/nature03895 [DOI] [PubMed] [Google Scholar]
  • 15.Meyers BC, Tingey S V, Morgante M. Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res. Cold Spring Harbor Lab; 2001;11: 1660–1676. doi: 10.1101/gr.188201 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Charles M, Belcram H, Just J, Huneau C, Viollet A, Couloux A, et al. Dynamics and differential proliferation of transposable elements during the evolution of the B and A genomes of wheat. Genetics. Oxford University Press; 2008;180: 1071–1086. doi: 10.1534/genetics.108.092304 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Doebley J, Stec A, Gustus C. teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics. Genetics Soc America; 1995;141: 333–346. Available: https://www.genetics.org/content/141/1/333.short doi: 10.1093/genetics/141.1.333 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Kobayashi S, Goto-Yamamoto N, Hirochika H. Retrotransposon-induced mutations in grape skin color. Science (80-). Citeseer; 2004;304: 982. doi: 10.1126/science.1095011 [DOI] [PubMed] [Google Scholar]
  • 19.Kawase M, Fukunaga K, Kato K. Diverse origins of waxy foxtail millet crops in East and Southeast Asia mediated by multiple transposable element insertions. Mol Genet Genomics. Springer; 2005;274: 131–140. doi: 10.1007/s00438-005-0013-8 [DOI] [PubMed] [Google Scholar]
  • 20.Butelli E, Licciardello C, Zhang Y, Liu J, Mackay S, Bailey P, et al. Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell. Am Soc Plant Biol; 2012;24: 1242–1255. doi: 10.1105/tpc.111.095232 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Yao J-L, Dong Y-H, Morris BAM. Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proc Natl Acad Sci. National Acad Sciences; 2001;98: 1306–1311. doi: 10.1073/pnas.031502498 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Zhang L, Hu J, Han X, Li J, Gao Y, Richards CM, et al. A high-quality apple genome assembly reveals the association of a retrotransposon and red fruit colour. Nat Commun. Nature Publishing Group; 2019;10: 1–13. doi: 10.1038/s41467-018-07882-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Paszkowski J. Controlled activation of retrotransposition for plant breeding. Curr Opin Biotechnol. Elsevier; 2015;32: 200–206. doi: 10.1016/j.copbio.2015.01.003 [DOI] [PubMed] [Google Scholar]
  • 24.Rey O, Danchin E, Mirouze M, Loot C, Blanchet S. Adaptation to global change: a transposable element—epigenetics perspective. Trends Ecol Evol. Elsevier; 2016;31: 514–526. doi: 10.1016/j.tree.2016.03.013 [DOI] [PubMed] [Google Scholar]
  • 25.Thieme M, Lanciano S, Balzergue S, Daccord N, Mirouze M, Bucher E. Inhibition of RNA polymerase II allows controlled mobilisation of retrotransposons for plant breeding. Genome Biol. 2017;18: 134. doi: 10.1186/s13059-017-1265-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Thieme M, Bucher E. Chapter Six—Transposable Elements as Tool for Crop Improvement. In: Mirouze M, Bucher E, Gallusci P, editors. Plant Epigenetics Coming of Age for Breeding Applications. Academic Press; 2018. pp. 165–202. 10.1016/bs.abr.2018.09.001 [DOI] [Google Scholar]
  • 27.Toker C, Berger J, Eker T, Sari D, Sari H, Gokturk RS, et al. Cicer turcicum: A New Cicer Species and Its Potential to Improve Chickpea. Front Plant Sci. Frontiers; 2021;12: 587. doi: 10.3389/fpls.2021.662891 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Jukanti AK, Gaur PM, Gowda CLL, Chibbar RN. Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. Br J Nutr. Cambridge University Press; 2012;108: S11–S26. doi: 10.1017/S0007114512000797 [DOI] [PubMed] [Google Scholar]
  • 29.FAOSTAT [Internet]. [cited 10 Jan 2021]. Available: http://www.fao.org/faostat/en/#data/QC
  • 30.Varshney RK, Song C, Saxena RK, Azam S, Yu S, Sharpe a G, et al. Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol. 2013;31: 240–246. doi: 10.1038/nbt.2491 [DOI] [PubMed] [Google Scholar]
  • 31.Parween S, Nawaz K, Roy R, Pole AK, Venkata Suresh B, Misra G, et al. An advanced draft genome assembly of a desi type chickpea (Cicer arietinum L.). Sci Rep. 2015;5: 12806. doi: 10.1038/srep12806 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Jain M, Misra G, Patel RK, Priya P, Jhanwar S, Khan AW, et al. A draft genome sequence of the pulse crop chickpea (C icer arietinum L.). Plant J. Wiley Online Library; 2013;74: 715–729. doi: 10.1111/tpj.12173 [DOI] [PubMed] [Google Scholar]
  • 33.Gupta S, Nawaz K, Parween S, Roy R, Sahu K, Kumar Pole A, et al. Draft genome sequence of Cicer reticulatum L., the wild progenitor of chickpea provides a resource for agronomic trait improvement. Dna Res. Oxford University Press; 2017;24: 1–10. doi: 10.1093/dnares/dsw042 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.NCBI. No Title [Internet]. Available: https://www.ncbi.nlm.nih.gov/assembly/GCA_002896215.2
  • 35.Varshney RK, Thudi M, Roorkiwal M, He W, Upadhyaya HD, Yang W, et al. Resequencing of 429 chickpea accessions from 45 countries provides insights into genome diversity, domestication and agronomic traits. Nat Genet. Nature Publishing Group; 2019;51: 857–864. doi: 10.1038/s41588-019-0401-3 [DOI] [PubMed] [Google Scholar]
  • 36.Gaur R, Verma S, Pradhan S, Ambreen H, Bhatia S. A high-density SNP-based linkage map using genotyping-by-sequencing and its utilization for improved genome assembly of chickpea (Cicer arietinum L.). Funct Integr Genomics. Springer; 2020;20: 763–773. doi: 10.1007/s10142-020-00751-y [DOI] [PubMed] [Google Scholar]
  • 37.Varshney RK, Thudi M, Muehlbauer FJ. The chickpea genome: An introduction. The Chickpea Genome. Springer; 2017. pp. 1–4. 10.1007/978-3-319-66117-9_1 [DOI] [Google Scholar]
  • 38.Lehti-Shiu MD, Panchy N, Wang P, Uygun S, Shiu S-H. Diversity, expansion, and evolutionary novelty of plant DNA-binding transcription factor families. Biochim Biophys Acta (BBA)-Gene Regul Mech. Elsevier; 2017;1860: 3–20. 10.1016/j.bbagrm.2016.08.005 [DOI] [PubMed] [Google Scholar]
  • 39.Doddamani D, Katta MA, Khan AW, Agarwal G, Shah TM, Varshney RK. CicArMiSatDB: the chickpea microsatellite database. BMC Bioinformatics. 2014;15: 212. doi: 10.1186/1471-2105-15-212 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Doddamani D, Khan AW, Katta MAVSK, Agarwal G, Thudi M, Ruperao P, et al. CicArVarDB: SNP and InDel database for advancing genetics research and breeding applications in chickpea. Database. 2015;2015. doi: 10.1093/database/bav078 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Verma M, Kumar V, Patel RK, Garg R, Jain M. CTDB: An Integrated Chickpea Transcriptome Database for Functional and Applied Genomics. PLoS One. 2015;10: e0136880. doi: 10.1371/journal.pone.0136880 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Li S, Liu L, Zhuang X, Yu Y, Liu X, Cui X, et al. MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell. Elsevier; 2013;153: 562–574. doi: 10.1016/j.cell.2013.04.005 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Vieira LM, Grativol C, Thiebaut F, Carvalho TG, Hardoim PR, Hemerly A, et al. PlantRNA_Sniffer: a SVM-based workflow to predict Long Intergenic non-coding RNAs in plants. Non-coding RNA. Multidisciplinary Digital Publishing Institute; 2017;3: 11. doi: 10.3390/ncrna3010011 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Satheesh V, Fan W, Chu J, Cho J. Recent advancement of NGS technologies to detect active transposable elements in plants. Genes Genomics. Springer; 2021; 1–6. doi: 10.1007/s13258-020-01012-9 [DOI] [PubMed] [Google Scholar]
  • 45.Jain M, Chevala VVSN, Garg R. Genome-wide discovery and differential regulation of conserved and novel microRNAs in chickpea via deep sequencing. J Exp Bot. Oxford University Press UK; 2014;65: 5945–5958. doi: 10.1093/jxb/eru333 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Gayali S, Acharya S, Lande NV, Pandey A, Chakraborty S, Chakraborty N. CicerTransDB 1.0: a resource for expression and functional study of chickpea transcription factors. BMC Plant Biol. 2016;16: 169. doi: 10.1186/s12870-016-0860-y [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Singh U, Khemka N, Rajkumar MS, Garg R, Jain M. PLncPRO for prediction of long non-coding RNAs (lncRNAs) in plants and its application for discovery of abiotic stress-responsive lncRNAs in rice and chickpea. Nucleic Acids Res. 2017;45: e183–e183. doi: 10.1093/nar/gkx866 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Jurka J, Kapitonov V V, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. Karger Publishers; 2005;110: 462–467. doi: 10.1159/000084979 [DOI] [PubMed] [Google Scholar]
  • 49.Llorens C, Futami R, Covelli L, Domínguez-Escribá L, Viu JM, Tamarit D, et al. The Gypsy Database (GyDB) of mobile genetic elements: release 2.0. Nucleic Acids Res. Oxford University Press; 2010;39: D70–D74. doi: 10.1093/nar/gkq1061 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Nussbaumer T, Martis MM, Roessner SK, Pfeifer M, Bader KC, Sharma S, et al. MIPS PlantsDB: a database framework for comparative plant genome research. Nucleic Acids Res. Oxford University Press; 2012;41: D1144–D1151. doi: 10.1093/nar/gks1153 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Amselem J, Cornut G, Choisne N, Alaux M, Alfama-Depauw F, Jamilloux V, et al. RepetDB: a unified resource for transposable element references. Mob DNA. Springer; 2019;10: 1–8. doi: 10.1186/s13100-018-0144-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Chaparro C, Guyot R, Zuccolo A, Piégu B, Panaud O. RetrOryza: a database of the rice LTR-retrotransposons. Nucleic Acids Res. Oxford University Press; 2007;35: D66–D70. doi: 10.1093/nar/gkl780 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Xu H-E, Zhang H-H, Xia T, Han M-J, Shen Y-H, Zhang Z. BmTEdb: a collective database of transposable elements in the silkworm genome. Database. Oxford Academic; 2013;2013. doi: 10.1093/database/bat055 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Murukarthick J, Sampath P, Lee SC, Choi B-S, Senthil N, Liu S, et al. BrassicaTED-a public database for utilization of miniature transposable elements in Brassica species. BMC Res Notes. BioMed Central; 2014;7: 1–11. doi: 10.1186/1756-0500-7-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Ma B, Li T, Xiang Z, He N. MnTEdb, a collective resource for mulberry transposable elements. Database. Oxford Academic; 2015;2015. doi: 10.1093/database/bav004 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Yadav CB, Bonthala VS, Muthamilarasan M, Pandey G, Khan Y, Prasad M. Genome-wide development of transposable elements-based markers in foxtail millet and construction of an integrated database. DNA Res. 2014;22: 79–90. doi: 10.1093/dnares/dsu039 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57.Lorenzetti APR, De Antonio GYA, Paschoal AR, Domingues DS. PlanTE-MIR DB: a database for transposable element-related microRNAs in plant genomes. Funct Integr Genomics. Springer; 2016;16: 235–242. doi: 10.1007/s10142-016-0480-5 [DOI] [PubMed] [Google Scholar]
  • 58.Yi F, Jia Z, Xiao Y, Ma W, Wang J. SPTEdb: a database for transposable elements in salicaceous plants. Database. Oxford Academic; 2018;2018. doi: 10.1093/database/bay024 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Yi F, Ling J, Xiao Y, Zhang H, Ouyang F, Wang J. ConTEdb: a comprehensive database of transposable elements in conifers. Database. Oxford Academic; 2018;2018. doi: 10.1093/database/bay131 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Ou S, Su W, Liao Y, Chougule K, Agda JRA, Hellinga AJ, et al. Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol. BioMed Central; 2019;20: 1–18. doi: 10.1186/s13059-018-1612-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.NCBI FTP server [Internet]. [cited 6 May 2020]. Available: ftp://ftp.ncbi.nlm.nih.gov/
  • 62.Ellinghaus D, Kurtz S, Willhoeft U. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics. Springer; 2008;9: 1–14. doi: 10.1186/1471-2105-9-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63.Xu Z, Wang H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 2007;35: W265–W268. doi: 10.1093/nar/gkm286 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Ou S, Jiang N. LTR_retriever: a highly accurate and sensitive program for identification of long terminal repeat retrotransposons. Plant Physiol. American Society of Plant Biologists; 2018;176: 1410–1422. doi: 10.1104/pp.17.01310 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Shi J, Liang C. Generic Repeat Finder: a high-sensitivity tool for genome-wide de novo repeat detection. Plant Physiol. American Society of Plant Biologists; 2019;180: 1803–1815. doi: 10.1104/pp.19.00386 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66.Su W, Gu X, Peterson T. TIR-learner, a new ensemble method for TIR transposable element annotation, provides evidence for abundant new transposable elements in the maize genome. Mol Plant. Elsevier; 2019;12: 447–460. doi: 10.1016/j.molp.2019.02.008 [DOI] [PubMed] [Google Scholar]
  • 67.Xiong W, He L, Lai J, Dooner HK, Du C. HelitronScanner uncovers a large overlooked cache of Helitron transposons in many plant genomes. Proc Natl Acad Sci. National Acad Sciences; 2014;111: 10263–10268. doi: 10.1073/pnas.1410068111 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 68.Smit AFA, Hubley R, Green P. RepeatModeler Open-1.0 (2008–2015). In: Seattle, USA: Institute for Systems Biology. [Internet]. 2015. p. 2018. Available: http://www.repeatmasker.org/RepeatModeler/ [Google Scholar]
  • 69.Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. Oxford university press; 1994;22: 4673–4680. doi: 10.1093/nar/22.22.4673 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 70.Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. Springer; 1980;16: 111–120. Available: https://link.springer.com/content/pdf/10.1007/BF01731581.pdf [DOI] [PubMed] [Google Scholar]
  • 71.Zhang Z, Li J, Zhao X-Q, Wang J, Wong GK-S, Yu J. KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics. Elsevier; 2006;4: 259–263. doi: 10.1016/S1672-0229(07)60007-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Koch MA, Haubold B, Mitchell-Olds T. Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol. Oxford University Press; 2000;17: 1483–1498. doi: 10.1093/oxfordjournals.molbev.a026248 [DOI] [PubMed] [Google Scholar]
  • 73.González LG, Deyholos MK. Identification, characterization and distribution of transposable elements in the flax (Linum usitatissimum L.) genome. BMC Genomics. 2012;13: 644. doi: 10.1186/1471-2164-13-644 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 74.Marcon HS, Domingues DS, Silva JC, Borges RJ, Matioli FF, de Mattos Fontes MR, et al. Transcriptionally active LTR retrotransposons in Eucalyptus genus are differentially expressed and insertionally polymorphic. BMC Plant Biol. BioMed Central; 2015;15: 1–16. doi: 10.1186/s12870-014-0410-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 75.UniProtKB [Internet]. Available: https://www.uniprot.org/uploadlists/
  • 76.Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, et al. The STRING database in 2017: quality-controlled protein–protein association networks, made broadly accessible. Nucleic Acids Res. 2016;45: D362–D368. doi: 10.1093/nar/gkw937 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77.Doncheva NT, Morris JH, Gorodkin J, Jensen LJ. Cytoscape StringApp: Network Analysis and Visualization of Proteomics Data. J Proteome Res. American Chemical Society; 2019;18: 623–632. doi: 10.1021/acs.jproteome.8b00702 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 78.Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks. Genome Res. 2003;13: 2498–2504. doi: 10.1101/gr.1239303 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79.Buels R, Yao E, Diesh CM, Hayes RD, Munoz-Torres M, Helt G, et al. JBrowse: a dynamic web platform for genome visualization and analysis. Genome Biol. 2016;17: 66. doi: 10.1186/s13059-016-0924-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80.Kaul Samir and Koo Hean L and Jenkins Jennifer and Rizzo Michael and Rooney Timothy and Tallon Luke J and Feldblyum, et al. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000;408: 796–815. doi: 10.1038/35048692 [DOI] [PubMed] [Google Scholar]
  • 81.Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, et al. The B73 maize genome: complexity, diversity, and dynamics. Science (80-). 2009;326: 1112–1115. doi: 10.1126/science.1178534 [DOI] [PubMed] [Google Scholar]
  • 82.Su W, Ou S, Hufford MB, Peterson T. A Tutorial of EDTA: Extensive De Novo TE Annotator. Plant Transposable Elem. Springer; 2021; 55–67. doi: 10.1007/978-1-0716-1134-0_4 [DOI] [PubMed] [Google Scholar]
  • 83.Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, Casagrande A, et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007;449: 463–467. doi: 10.1038/nature06148 [DOI] [PubMed] [Google Scholar]
  • 84.Argout X, Salse J, Aury J-M, Guiltinan MJ, Droc G, Gouzy J, et al. The genome of Theobroma cacao. Nat Genet. 2011;43: 101–108. doi: 10.1038/ng.736 [DOI] [PubMed] [Google Scholar]
  • 85.Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, et al. The genome of the cucumber, Cucumis sativus L. Nat Genet. 2009;41: 1275–1281. doi: 10.1038/ng.475 [DOI] [PubMed] [Google Scholar]
  • 86.Zhao D, Ferguson AA, Jiang N. What makes up plant genomes: The vanishing line between transposable elements and genes. Biochim Biophys Acta—Gene Regul Mech. 2016;1859: 366–380. doi: 10.1016/j.bbagrm.2015.12.005 [DOI] [PubMed] [Google Scholar]
  • 87.SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL. The paleontology of intergene retrotransposons of maize. Nat Genet. 1998;20: 43–45. doi: 10.1038/1695 [DOI] [PubMed] [Google Scholar]
  • 88.Da Costa ZP, Cauz-Santos LA, Ragagnin GT, Van Sluys M-A, Dornelas MC, Berges H, et al. Transposable element discovery and characterization of LTR-retrotransposon evolutionary lineages in the tropical fruit species Passiflora edulis. Mol Biol Rep. 2019;46: 6117–6133. doi: 10.1007/s11033-019-05047-4 [DOI] [PubMed] [Google Scholar]
  • 89.Ladizinsky G, Adler A. The origin of chickpea Cicer arietinum L. Euphytica. 1976;25: 211–217. 10.1007/BF00041547 [DOI] [Google Scholar]
  • 90.Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature. 2011;472: 115–119. doi: 10.1038/nature09861 [DOI] [PubMed] [Google Scholar]
  • 91.Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR. Pack-MULE transposable elements mediate gene evolution in plants. Nature. 2004;431: 569–573. doi: 10.1038/nature02953 [DOI] [PubMed] [Google Scholar]
  • 92.Nekrutenko A, Li W-H. Transposable elements are found in a large number of human protein-coding genes. Trends Genet. 2001;17: 619–621. doi: 10.1016/s0168-9525(01)02445-3 [DOI] [PubMed] [Google Scholar]
  • 93.Britten R. Transposable elements have contributed to thousands of human proteins. Proc Natl Acad Sci. National Academy of Sciences; 2006;103: 1798–1803. doi: 10.1073/pnas.0510007103 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 94.Lipatov M, Lenkov K, Petrov DA, Bergman CM. Paucity of chimeric gene-transposable element transcripts in the Drosophila melanogaster genome. BMC Biol. 2005;3: 24. doi: 10.1186/1741-7007-3-24 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 95.Lockton S, Gaut BS. The Contribution of Transposable Elements to Expressed Coding Sequence in Arabidopsis thaliana. J Mol Evol. 2009;68: 80–89. doi: 10.1007/s00239-008-9190-5 [DOI] [PubMed] [Google Scholar]
  • 96.Pereira V. Insertion bias and purifying selection of retrotransposons in the Arabidopsis thalianagenome. Genome Biol. 2004;5: R79. doi: 10.1186/gb-2004-5-10-r79 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 97.Cresse AD, Hulbert SH, Brown WE, Lucas JR, Bennetzen JL. Mu1-related transposable elements of maize preferentially insert into low copy number DNA. Genetics. 1995;140: 315–324. doi: 10.1093/genetics/140.1.315 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 98.SanMiguel P, Tikhonov A, Jin Y-K, Motchoulskaia N, Zakharov D, Melake-Berhan A, et al. Nested Retrotransposons in the Intergenic Regions of the Maize Genome. Science (80-). 1996;274: 765–768. doi: 10.1126/science.274.5288.765 [DOI] [PubMed] [Google Scholar]
  • 99.Hollister JD, Gaut BS. Epigenetic silencing of transposable elements: A trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res. 2009;19: 1419–1428. doi: 10.1101/gr.091678.109 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 100.Bennetzen JL. The contributions of retroelements to plant genome organization, function and evolution. Trends Microbiol. 1996;4: 347–353. doi: 10.1016/0966-842x(96)10042-1 [DOI] [PubMed] [Google Scholar]
  • 101.Rossi M, Araujo PG, Van Sluys M-A. Survey of transposable elements in sugarcane expressed sequence tags (ESTs). Genet Mol Biol. SciELO Brasil; 2001;24: 147–154. 10.1590/S1415-47572001000100020 [DOI] [Google Scholar]
  • 102.Hoen DR, Park KC, Elrouby N, Yu Z, Mohabir N, Cowan RK, et al. Transposon-Mediated Expansion and Diversification of a Family of ULP-like Genes. Mol Biol Evol. 2006;23: 1254–1268. doi: 10.1093/molbev/msk015 [DOI] [PubMed] [Google Scholar]
  • 103.Doyle O, Corden JL, Murphy C, Gall JG. The distribution of RNA polymerase II largest subunit (RPB1) in the Xenopus germinal vesicle. J Struct Biol. 2002;140: 154–166. doi: 10.1016/s1047-8477(02)00547-6 [DOI] [PubMed] [Google Scholar]
  • 104.Kunze R, Saedler H, Lönnig W-E. Plant Transposable Elements. In: Callow JA, editor. Classic Papers. Academic Press; 1997. pp. 331–470. 10.1016/S0065-2296(08)60284-0 [DOI] [Google Scholar]
  • 105.Sawicka A, Villamil G, Lidschreiber M, Darzacq X, Dugast-Darzacq C, Schwalb B, et al. Transcription activation depends on the length of the RNA polymerase II C-terminal domain. EMBO J. 2021;40: e107015. doi: 10.15252/embj.2020107015 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 106.Peng Y, Zhou P, Zhao J, Li J, Lai S, Tinker NA, et al. Phylogenetic relationships in the genus Avena based on the nuclear Pgk1 gene. PLoS One. Public Library of Science; 2018;13: 1–18. doi: 10.1371/journal.pone.0200047 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 107.Tang C, Qi J, Chen N, Sha L-N, Wang Y, Zeng J, et al. Genome origin and phylogenetic relationships of Elymus villosus (Triticeae: Poaceae) based on single-copy nuclear Acc1, Pgk1, DMC1 and chloroplast trnL-F sequences. Biochem Syst Ecol. 2017;70: 168–176. 10.1016/j.bse.2016.11.011 [DOI] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Fig. The distribution of C. echinospermum TEs superfamilies according to their length.

(TIF)

Click here for additional data file. (990.2KB, tif)
S2 Fig. The distribution of C. reticulatum TEs superfamilies according to their length.

(TIF)

Click here for additional data file. (950.6KB, tif)
S3 Fig. Gene ontology of 315 C. arietinum TE-gene chimeras assigned to 486 molecular functions GO terms.

(TIF)

Click here for additional data file. (338.6KB, tif)
S4 Fig. Gene ontology of 215 C. arietinum TE-gene chimeras assigned to 325 cellular components GO terms.

(TIF)

Click here for additional data file. (537.3KB, tif)
S5 Fig. Protein-protein interaction for genes nearby TEs.

(TIF)

Click here for additional data file. (2.9MB, tif)
S6 Fig. Protein-protein interaction for both TE-gene chimeras and genes nearby TEs.

(TIF)

Click here for additional data file. (5.1MB, tif)
S7 Fig. CicerSpTEdb’s statistics page.

(TIF)

Click here for additional data file. (748.5KB, tif)
S8 Fig. CicerSpTEdb’s comparisons page.

(TIF)

Click here for additional data file. (895.2KB, tif)
S9 Fig. CicerSpTEdb’s bulk download page.

(TIF)

Click here for additional data file. (1.3MB, tif)
S1 Table. The details of the identified TEs in C. arietinum, including the chromosome/scaffold id, TE start and end position in the genome, TE corresponding superfamily, and TE length.

(XLSX)

Click here for additional data file. (97.2KB, xlsx)
S2 Table. The details of the identified TEs in C. reticulatum, including the chromosome/scaffold id, TE start and end position in the genome, TE corresponding superfamily, and TE length.

(XLSX)

Click here for additional data file. (161.4KB, xlsx)
S3 Table. The details of the identified TEs in C. echinospermum, including the chromosome/scaffold id, TE start and end position in the genome, TE corresponding superfamily, and TE length.

(XLSX)

Click here for additional data file. (165.9KB, xlsx)
S4 Table. The details of the identified TEs that located near genes in C. arietinum.

(XLSX)

Click here for additional data file. (68.1KB, xlsx)
S1 File. The programs and their parameters used for identification of TEs in Cicer species.

(DOCX)

Click here for additional data file. (23.5KB, docx)

Data Availability Statement

All relevant data are within the manuscript, Supporting Information files, and CicerSpTEdb is freely available at http://cicersptedb.easyomics.org/.

Articles from PLoS ONE are provided here courtesy of PLOS

RESOURCES