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Construction of a comprehensive library of repeated sequences for the annotation of Citrus genomes

BMC Genomic Data volume 26, Article number: 30 (2025) Cite this article

Abstract

Background

The comprehensive annotation of repeated sequences in genomes is an essential prerequisite for studying the dynamics of these sequences over time and their involvement in gene regulation. Currently, the diversity of repeated sequences in Citrus genomes is only partially characterized because the annotations have been performed using heterogeneous bioinformatics tools, each with its specificity and dedicated only to the annotation of transposable elements.

Results

We combined complementary repeat-finding programs including REPET, CAULIFINDER, and TAREAN, to enable the identification of all types of repetitive sequences found in plant genomes, including transposable elements, endogenous caulimovirids, and satellite DNAs. A fine-grained annotation method was first developed to create a consensus sequence library of repeated sequences identified in the genome assemblies of C. medica, C. micrantha, C. reticulata, and C. maxima, the four ancestral parental species involved in the formation of economically valuable cultivated Citrus varieties. A second, faster annotation method was developed to enrich the dataset by adding new repeated sequences retrieved from genome assemblies of other Citrus species and closely related species belonging to the Aurantioideae subfamily. The final reference library contains 3,091 consensus sequences, of which 94.5% are transposable elements. The diversity of endogenous caulimovirids was characterized for the first time within the genus Citrus, contributing 160 consensus sequences to the final reference library. Finally, 10 satellite DNAs were also identified.

Conclusion

Combining multiple repeat detection methods enables the comprehensive annotation of all repeated sequences in Citrus genomes. Using the final reference library reported in this work will improve our understanding of the dynamics of repeated sequences during Citrus speciation, particularly following the genome duplication and hybridization events that led to modern cultivars. The exploration of repeat position insertions along chromosomes using the developed web interface, RepeatLoc Citrus, will also make it possible to further investigate the role of transposable elements and endogenous caulimovirids in genome structure and gene regulation in Citrus species.

Peer Review reports

Background

Over the last two decades, cost reductions and improvements in DNA sequencing technologies have led to an exponential increase in plant genome assemblies [1]. This trend has stimulated the development of several bioinformatics tools dedicated to the annotation of repetitive sequences, also known as the “repeatome”, which represent a significant fraction of most eukaryotic genomes [2]. The characterization of repeated sequences has revealed their ubiquity in plant genomes [3,4,5,6]. Transposable elements (TEs) are genetic sequences that can replicate in large numbers and insert into chromosomes [7,8,9]. Initially dismissed as “junk DNA”, TEs are now recognized as key players in genome dynamics and species evolution [10]. In many plants, they have contributed to the emergence of new phenotypes by acting as cis-regulatory elements, modifying the chromatin landscape around genes, mediating gene duplication, and disrupting coding sequences [6, 11,12,13]. For example, TE insertions have been linked to variation in the fruit color of Chardonnay grape clones [14] or to sex determination in melon [15]. In tomato, the elongated fruit phenotype has been linked to a TE-mediated duplication of the SUN locus [16], and the yellow color of fruit flesh in several genotypes has been linked to a TE insertion in the PSY1 locus [17]. Recent studies have demonstrated the involvement of TEs in the variation of key agronomic traits in maize and rice species and confirmed the need to take them into account when breeding new varieties [18,19,20,21]. Satellite DNAs, or long tandem repeats, are also found in plant genomes, particularly at centromeres, but are sometimes concentrated in other specific chromosomal regions [22,23,24]. Unlike TEs, they cannot self-replicate, but unequal recombination during meiosis and polymerase replication splicing contribute to their accumulation in large numbers in genomes [25]. They are mainly involved in genome structure and chromosome stability by participating in the formation of heterochromatin. In addition to TEs and satellite DNAs, plant genomes often contain endogenous caulimovirids (ECVs), another class of repetitive DNA sequences [26]. ECVs result from the integration of genomic sequences from members of the viral family Caulimoviridae during infections [27,28,29,30]. Their integration into their host genomes is not an obligatory step in their replication cycle but is thought to occur during the repair of DNA breaks [26]. To date, their role in the structure and evolution of plant genomes is poorly understood.

It is well established that repeated sequences such as TEs play a role in genomic structural variations causing phenotypic variations observed in vegetatively propagated crops [19, 31, 32]. The phenotypic diversity observed in sweet orange cultivars has been directly linked to specific TE insertions near host genes and shown to be involved in traits such as blood color, apomixis, and acidity changes [33,34,35,36,37,38,39]. Given the high economic value of citrus fruits, with an annual production of over 100 million tons in 2023, there is a particular relevance in integrating repeatome annotation data into breeding schemes for new citrus varieties [40, 41]. Whole genome annotations of repetitive sequences have been achieved for several Citrus spp., but further analyses showed that only a fraction of the repeated sequences were identified. Indeed, retrotransposons, LINEs (long interspersed nuclear elements), and MITEs (miniature inverted repeat transposable elements) were best characterized, but their estimated abundances in the analyzed genomes depended on the annotation methods and the quality of genome assemblies. For example, in sweet orange (C. x aurantium var. sinensis), the relative amount of Copia and Gypsy elements varies between 15.3% and 24.2% of the genome according to the different annotation methods used [38, 39, 42,43,44]. Other types of TEs, such as Helitrons and SINEs, remain to be fully identified, resulting in an underestimation of their abundance and diversity. Furthermore, the diversity of ECVs within Citrus genomes has not been comprehensively determined. However, several studies have indicated their relatively high density in sweet oranges, at 2.3 copies per Mb, compared with an average of 0.2 copies per Mb in the genomes of other seed plants [29, 45].

In this context, our main objective is to determine the comprehensive diversity of repeated sequences in the genomes of Citrus spp. and related species from the Aurantioideae subfamily through the annotation of TEs, ECVs, and satellite DNAs (especially macrosatellites). Using several pipelines, two complementary annotation methods were developed to construct a reference consensus sequence library that is representative of the repeated sequences found in the genomes of primitive, wild, and cultivated Citrus spp. [46,47,48]. It is anticipated that this library will serve as a gold standard for the annotation of Citrus genomes, which will facilitate the study of the insertion dynamics of repeated sequences and their roles in genome structure and clonal variation in this botanical genus.

Development of a Citrus reference library

Fine-grained annotation of transposable elements (TEs)

We performed a fine-grained annotation of the repeated sequences found in the genome assemblies of the four ancestral taxa C. medica, C. micrantha, C. reticulata, and C. maxima, which are the progenitors of the major cultivated citrus varieties [46, 49] (Fig. 1; Table 1). This annotation was first implemented on genome assemblies for each progenitor using the REPET v3.0 package [50,51,52]. According to statistics of assembly data, only a subgenome was analyzed for each species. These subgenomes are made up of “virtual contigs” or “chunks” obtained by removing stretches of > 11 undefined bases (Ns) to exclude gaps in these sequences. Only chunks longer than 500 kbp in C. medica and chunks longer than 100 kbp in C. micrantha, C. reticulata, and C. maxima were conserved, covering 93–96% of the genome assemblies. The REPET TEdenovo pipeline was used to detect all repeated sequences in the subgenomes and to generate libraries of consensus sequences representative of each TE family (setting parameters: at least 3 sequences per group, Grouper, Recon, and Piler clustering, no remove redundancy). The consensus sequences were then classified with the PASTEC classifier (included in the TEdenovo pipeline [52]) according to structural and functional features based on characterized TEs from the RepBase23.12 database [53, 54], the library of profiles from Pfam32.0 [55] and the GyDB2.0 database [56] specially formatted for REPET. All consensus sequences classified as simple sequence repeats (SSR), rDNA, potential host genes (PHG; containing host gene Pfam domains), and unclassified sequences built with less than 10 copies per cluster were removed from the TE libraries. After filtering, TE libraries of 13,483, 10,957, 11,451, and 12,958 consensus sequences were obtained for C. medica, C. micrantha, C. reticulata, and C. maxima, respectively (Fig. 1). Each TE library was used to annotate the genome assembly from which it was generated, using the TEannot pipeline included in REPET (default parameters). This step resulted in an estimated TE coverage of 56% in C. medica, 51% in C. micrantha, 52% in C. reticulata, and 55% in C. maxima. To refine the annotation of TEs, TE libraries were again filtered to retain only consensus sequences with at least one full-length fragment (FLF) in the genome (i.e. a fragment covering more than 95% of the consensus sequences), and then a second TEannot run was performed. This iterative process resulted in the filtered TE libraries of 3,579, 4,469, 4,427, and 3,834 consensus sequences for C. medica, C. micrantha, C. reticulata, and C. maxima, respectively, with a reduced TE coverage of 1–3% depending on the species (Fig. 1). All consensus sequences were manually curated using copy coverage plots, structural and functional features (ORFs, tandem repeats, polyA tail, protein domain HMM profiles, SSR, and BLAST results), and MCL clustering. This manual curation allowed us to classify some TEs at the family level, identify ECVs that would otherwise be automatically classified as TEs, and reclassify some inaccurately classified consensus sequences (Additional files 2 and 3). To reduce intra-species redundancy, consensus sequences that fully aligned to a longer other consensus sequence with an identity greater than 80% were removed from each TE library following the Wickers’ rule [8] and using Cd-hit v. 4.8.1 [57].

Fig. 1
figure 1

Schematic representation of the fine-grained method employed for de novo annotation of repeated sequences in the four ancestral Citrus taxa C. medica, C. micrantha, C. reticulata, and C. maxima. Results from the different bioinformatics tools REPET, EDTA, MUST, TAREAN, and CAULIFINDER were combined to produce a reference fine-grained annotation library of 2,883 consensus sequences representative of the diversity of all repeated sequences retrieved in Citrus. The numbers shown in the species-specific colored boxes indicate the number of consensus sequences and their genome coverage obtained using the TEannot pipeline. ECV: Endogenous Caulimovirid element; FLF: Full Length Fragment; PHG: Potential Host Gene; rDNA: ribosomal DNA; SSR: Simple Sequence Repeat; TE: Transposable Element

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Table 1 List of the genome assemblies used for annotating repeated sequences
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In addition to REPET, several other TE detection programs were used. First, the EDTA pipeline [65] was launched on the four genomes to validate the structure of the REPET predictions and to solve annotation conflicts encountered with the PASTEC classifier. Consensus sequences generated using EDTA and qualified as Helitron were specifically studied. Their structures were confirmed using DANTE, the TE protein domain identification tool included in the RepeatExplorer pipeline [66], and novel Helitrons were added to the TE libraries. In parallel, the four Citrus assemblies were analyzed using a collection of TE structure-based tools, including LTR_STRUC searching for LTR retrotransposons [67], MUSTv2, MITE-Hunter searching for MITEs [68, 69], and SINE-Finder searching for short interspersed nuclear elements (SINEs) [70]. For each Citrus species, these newly detected consensus were added to the respective TE libraries, and redundant sequences were filtered out using Cd-hit with the same parameters as above.

Finally, the four TE libraries were combined, and interspecific redundancy was reduced using Cd-hit clustering. This resulted in a fine-grained annotation library of 2,875 consensus sequences representative of the diversity of TEs (2,720 consensus sequences) and ECVs (155 consensus sequences) found in the four ancestral Citrus taxa (Fig. 1, Additional file 1).

Annotation of endogenous caulimovirid sequences (ECVs)

Special attention was dedicated to the identification of ECVs. The 155 ECVs consensus sequences identified in the four ancestral taxa using the TEdenovo pipeline were included in the fine-grained annotation library (Fig. 1). During consensus sequence quality checks, sequences containing a movement protein domain (MP), which is a hallmark of Caulimoviridae genomes, were temporarily classified as ECVs. To confirm their classification as ECVs, the 155 consensus sequences were compared with the custom library of reverse transcriptase (RT) protein sequences from known caulimovirids and LTR retrotransposons used by CAULIFINDER, a pipeline specifically designed for the specific annotation of ECVs [71]. Consensus sequences displaying a best hit against caulimovirid RTs with e-values < 1e- 06 following BLASTx analyses were retained as ECVs in the fine-grained annotation library.

Annotation of satellite DNAs

Finally, satellite DNAs (tandem repeats) were identified using TAREAN [72] (Fig. 1). Briefly, this pipeline performs a graph-based clustering from libraries of paired-end Illumina reads. Clusters with circular topology are isolated, and monomer units of the satellite DNAs are characterized. For each ancestral taxon, a sample of 1 million paired-end reads was randomly extracted from Illumina libraries used for genome assemblies (Table 1) and analyzed by TAREAN. To avoid redundancy, satellite DNAs detected in the four genome assemblies were aligned with each other using BLASTn [73] and only those with sequence identity < 80% and e-values < 1e- 06 were conserved. In total, eight different satellite DNAs were identified and added to the fine-grained annotation library (Table 2, Additional file 1).

Table 2 Classification and number of repeated sequences included in the final reference library
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Enrichment of the fine-grained annotation library with repeated sequences from other Citrus and related species

To be more inclusive of the diversity of the repeated sequences found across the Citrus genus, we extended our search to the assembled genomes of 8 other Citrus species and two related species Atalantia buxifolia and Murraya koenigii (Table 1). A second, faster annotation method was developed to reduce the execution time compared to the fine-grained method (Fig. 2). This method uses the same combination of repeat-finding programs but skips some steps and uses the fine-grained annotation library as a reference. Firstly, the TEdenovo pipeline was used on DNA chunks longer than 20kbp, deriving from the sampling of the genome assemblies. The resulting consensus sequence libraries were filtered by removing PHG, rDNA, SSR sequences, and unclassified sequences built with < 10 copies per cluster as described above. In addition to the REPET pipeline, TAREAN, and MITE-Hunter were also used to annotate the satellite DNAs and the MITEs in each genome assembly, respectively. Using BLASTn, consensus sequences without sequence homology to TEs, ECVs, or satellite DNAs already present in the fine-grained annotation library were retained (setting parameters: < 80% of identity, e-value < 1e- 06). They were manually curated and classified as described above and then added to the fine-grained annotation library.

Fig. 2
figure 2

Schematic representation of the method used to annotate repeated sequences in other Citrus species and related species. Compared to the fine-grained method, multiple steps were skipped to reduce execution time, and the fine-grained annotation library was used as a reference. A final reference library of 3,116 consensus sequences was built containing the diversity of TEs, ECVs, and satellite DNAs identified in Citrus and related species

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The annotation of the 10 extra genomes using the faster method led to the identification of 208 additional new consensus sequences, corresponding to 201 TEs, 5 ECVs, and 2 satellite DNAs (Additional file 1). In total, the final reference library contains 3,091 consensus sequences representative of the diversity of repeated sequences, including 2,921 TEs (94.5%), 160 ECVs (5.2%), and 10 satellite DNAs ranging in size from 141 to 181 bp (0.3%) (Fig. 3; Table 2) [74]. Among annotated TEs, 1,905 consensus sequences are retrotransposons (Class I elements) and 949 are DNA transposons (Class II elements).

Fig. 3
figure 3

Classification of the repeated sequences contained in the final reference library. Numbers in parentheses refer to the number of consensus sequences and the associated percentage

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A benchmark for the annotation of repeated sequences in Citrus genomes and their role in genome dynamics

There is currently no standard method for the annotation of all repeated sequences in assembled genomes. Multiple bioinformatic programs can be used, but each has its own specificity, resulting in variable precision levels in the annotation, depending on the nature of the repeats. Here, we propose two complementary methods for the annotation of all repeated sequences in Citrus genomes, including TEs, ECVs, and satellite DNAs (Figs. 1 and 2). These annotation methods allowed us to construct the first comprehensive reference consensus sequence library of Citrus repeats. This final reference library paves the way to the accurate, reproducible, and standardized quantification of repeated sequences in Citrus genomes. Just as the fine-grained method can be reused to annotate repeated sequences in other plant genomes (Fig. 1), the final reference library can be enriched by annotating newly assembled Citrus genomes using the second, faster method described in this paper (Fig. 2). The final reference library contains the diversity of repeated sequences identified in twelve citrus species either from the divergent speciation including the four ancestral species (citron, papeda micrantha, wild mandarin, and pummelo), or from the reticulate speciation with the four cultivated species, sweet orange, clementine satsuma mandarin and limon. In future, the quick annotation of new assembled citrus genomes will facilitate repeated sequences detection and improved their study in citrus species.

In 2019, Liu et al. [75] annotated five different Citrus genomes (C. x aurantium var. sinensis, C. x aurantium var. clementina, C. medica, C. ichangensis and C. maxima) and built a library of 450 consensus sequences, including 340 L retrotransposons and 110 MITEs. We compared this library with our final reference library using BLASTn (e-value < 1e- 06). This comparison revealed that 423 of the 450 consensus sequences were common to both libraries, representing only 13.7% of the repeat diversity found in our final reference library (Fig. 4). The comparison showed that 45 consensus sequences from the study of Liu et al. were incorrectly classified (e.g. 7 MITEs consensus sequences corresponded to LTR retrotransposons, 6 L retrotransposon sequences corresponded to satellite DNAs, and 27 consensus sequences had no homology with either sequences of our final reference library or sequences in the RepBase23.12 database (BLASTn; e-value < 1e- 06). More recently, Wu et al. [76] developed a pan-genome TE library of 21,680 TEs consensus sequences based on the genome annotation of 14 Citrus and 6 related species, compared with our final reference library of 3,091 consensus repeated sequences from 14 Citrus and 2 related species. The sequence library of Wu et al. is unpublished, precluding its comparison with our final reference library. However, using seven times fewer consensus sequences, our library and method revealed the diversity of TEs, ECVs, and satellite DNAs found in Citrus spp.

Fig. 4
figure 4

Comparison of repeated sequences composing the final reference library of Citrus and the library generated by Liu et al. [75]. Horizontal bars represent the number of consensus sequences identified for each TE family, ECVs, or satellite DNAs in the final reference library (left) and in the Liu et al. library (right, classified according to best-hit match with the final reference library)

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The Citrus consensus sequence library developed in this study will significantly improve the study of the TEs, ECVs, and satellite DNAs dynamics in Citrus. It will enable the comparison of repeated sequence counts and locations in Citrus species that diverged following the allopatric speciation that occurred in the last 6–8 million years [48, 77]. The comparison of ancestral parental taxa and admixed species will also enable a better characterization of the consequences of hybridizations and whole genome duplication events on the dynamics of TEs [19, 78,79,80,81]. The tools and methods described in this paper could also help unravel the role of TEs and ECVs in some phenotypic variations observed in vegetatively propagated crops such as sweet oranges [34,35,36,37, 39]. Finally, the comprehensive annotation of ECVs in Citrus genomes will allow a better understanding of their putative role in genome architecture, gene regulation, and their integration dynamics in plant genomes.

RepeatLoc Citrus: visualize and explore the repeatome of the Citrus genomes

To enhance the study of repeated sequences in Citrus genomes, we developed an interface to visualize and analyze TEs, ECVs, and satellite DNAs along the nine chromosomes of the four Citrus ancestor species. This interface, called RepeatLoc Citrus, has been implemented through the Citrus Genome Hub (https://citrus-tools-genome-hub.southgreen.fr/repeatloc/; accessed 4 April 2025), a publicly available web portal that offers the possibility to study and compare the genomes of Citrus species. Following the selection of the query Citrus species, users can visualize the density and positions of repeated sequences along the chromosomes (Fig. 5). For each type of repeated sequence, the number of copies and their coverage on each chromosome is available from arborescent entries corresponding to the different levels of TEs, ECVs, and satellite DNA classification. Users can also explore specific positions on chromosomes and extract detailed information about genes and repeated sequences by following the link to the Genome Browser (JBrowse). The addition of new genome assemblies in future updates of RepeatLoc Citrus will strengthen the analysis of the repeatome within the Citrus genus.

Fig. 5
figure 5

Examples of Citrus repeatome exploration available on the RepeatLoc Citrus interface. a. Users can select the Citrus species (1) and the repeated sequences (2) they wish to localize on chromosomes. Information on density, number of copies, and genome coverage is displayed (3). A specific region can be studied by clicking and dragging with the mouse on the chromosome (4) or by querying its positions (1). The results are displayed below (5), showing the size and position of the copies in the selected window. Data on the selected window can be downloaded using the link to the JBrowse (6). b. Screenshot of the JBrowse obtained following the link (6). Users can compare the position of the genes (7) and the repeated sequences (8) found in the region of interest

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Conclusion

In this study, we combined several dedicated pipelines to build a final reference library of 3,091 consensus sequences representing the diversity of Citrus transposable elements, endogenous caulimovirids, and satellite DNAs. This library provides important resources for studying the dynamics of repeated sequences in Citrus genomes and their role in phenotypic variations and speciation. To complement the existing citrus databases on genomic, expression and variation data (https://www.citrusgenomedb.org/; http://citrus.hzau.edu.cn/; http://citgvd.cric.cn/home; http://www.orangeexpdb.com/, accessed 29 March 2025), the development of the online interface, RepeatLoc Citrus (tool included in the Citrus Genome Hub), will improve the localisation of repeated sequences along the chromosomes and highlight their putative involvement in altering gene regulation.

Data availability

The accession numbers of the genome assemblies used in this study are listed in Table 1. The final reference library generated in this study is available in the UR1390-AGAP Corse Dataverse (Data INRAE https://entrepot.recherche.data.gouv.fr/dataverse/inrae) at https://doiorg.publicaciones.saludcastillayleon.es/10.57745/ZVYEBU.

Abbreviations

ECV:

Endogenous Caulimovirid

EVE:

Endogenous Viral Element

FLF:

Full Length Fragment

LINE:

Long Interspersed Nuclear Element

LTR:

Long Terminal Repeat

MITE:

Miniature Inverted-repeat Transposable Element

PHG:

Potential Host Gene

rDNA:

Ribosomal DNA

SINE:

Short Interspersed Nuclear Element

SSR:

Simple Sequence Repeat

TE:

Transposable Element

TIR:

Terminal Inverted Repeat

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Acknowledgements

Thanks to Carole Quinton and Cointreau for their involvement in this project. Thanks to Raphaël Morillon and Claire Billot for their help in realizing this project. Thanks to the Citrus BRC for allowing us to study the genetic diversity of the genus Citrus by giving us access to different varieties of citrus fruit [82].

Funding

DG was financed by the BAP (Biologie et amélioration des Plantes) department of INRAE and the Rémy-Cointreau Company (Hesperides project). PYT was funded by the European Regional Development Fund (ERDF, contract REU005756) and Région Réunion through the project “Dispositif de partenariat en santé et biodiversité”.

This work has been realized with the support of MESO@LR-Platform at the University of Montpellier, with Cirad financial support and technical support from the bioinformatics group of the UMR AGAP Institute, member of the French Institute of Bioinformatics (IFB) - South Green Bioinformatics Platform. The CIRAD has subscribed an institutional license from https://phoenixbioinfo.org/repbase (ref:_00Do0J6b5._5001J10Do2W:ref; 07/23/2021-07/22/2024, access extended to 08/11/2024) to use the Repbase database v. 23.12 (https://www.girinst.org/repbase).

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Authors and Affiliations

  1. UR AGAP Corse, INRAE, Institut Agro, CIRAD, University of Montpellier, San Giuliano, F-20230, France

    Delphine Giraud, Gilles Costantino & François Luro

  2. URGI, INRAE, Université Paris-Saclay, Versailles, F-78026, France

    Nathalie Choisne, Héléna Vassilieff & Florian Maumus

  3. UMR AGAP, CIRAD, Institut Agro, INRAE, University of Montpellier, Montpellier, F-34060, France

    Marilyne Summo, Stéphanie Sidibe-Bocs, Gaetan Droc & Patrick Ollitrault

  4. UMR AGAP, CIRAD, Montpellier, F-34398, France

    Marilyne Summo, Stéphanie Sidibe-Bocs, Gaetan Droc & Patrick Ollitrault

  5. CIRAD, UMR PVBMT, Saint Pierre, La Réunion, F‐97410, France

    Pierre-Yves Teycheney

  6. UMR PVBMT, Université de la Réunion, Saint-Pierre de La Réunion, F-97410, France

    Pierre-Yves Teycheney

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  1. Delphine Giraud
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Contributions

DG: Conceptualization, Methodology, Data curation, Writing – original draft. NC: Methodology, Data curation, Writing – review & editing. SSB, GC, GD, and HV: Software, Validation, Data management. MS and GD: Development and deployment of the visualization tool RepeatLoc Citrus. PYT and FM: Writing – review & editing. PO: Conceptualization, Writing – review & editing. FL: Conceptualization, Funding acquisition, Writing – review & editing. All authors read and approved the final manuscript.

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Giraud, D., Choisne, N., Summo, M. et al. Construction of a comprehensive library of repeated sequences for the annotation of Citrus genomes. BMC Genom Data 26, 30 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12863-025-01321-6

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