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Nuclear and mitochondrial genomes of the hybrid fungal plant pathogen Verticillium longisporum display a mosaic structure

17 Jan 2018-bioRxiv (Cold Spring Harbor Laboratory)-pp 249565

TL;DR: In conclusion, the nuclear and mitochondrial genomes of V. longisporum parents interacted dynamically in the hybridization aftermath, and novel combinations of DNA sequence of different parental origin facilitated genome stability after hybridization and consecutive niche adaptation ofV.
Abstract: Allopolyploidization, genome duplication through interspecific hybridization, is an important evolutionary mechanism that can enable organisms to adapt to environmental changes or stresses. This increased adaptive potential of allopolyploids can be particularly relevant for plant pathogens in their quest for host immune response evasion. Allodiploidization likely caused the shift in host range of the fungal pathogen plant Verticillium longisporum, as V. longisporum mainly infects Brassicaceae plants in contrast to haploid Verticillium spp. In this study, we investigated the allodiploid genome structure of V. longisporum and its evolution in the hybridization aftermath. The nuclear genome of V. longisporum displays a mosaic structure, as numerous contigs consists of sections of both parental origins. V. longisporum encountered extensive genome rearrangements, whereas the contribution of gene conversion is negligible. Thus, the mosaic genome structure mainly resulted from genomic rearrangements between parental chromosome sets. Furthermore, a mosaic structure was also found in the mitochondrial genome, demonstrating its bi-parental inheritance. In conclusion, the nuclear and mitochondrial genomes of V. longisporum parents interacted dynamically in the hybridization aftermath. Conceivably, novel combinations of DNA sequence of different parental origin facilitated genome stability after hybridization and consecutive niche adaptation of V. longisporum.
Topics: Verticillium longisporum (71%), Genome (56%), Verticillium (52%), Genomics (51%), Nuclear gene (50%)

Summary (3 min read)

INTRODUCTION

  • Whole-genome duplication (WGD) is an important evolutionary mechanism that facilitates environmental adaptation (Van de Peer et al. 2017; Mallet 2005) .
  • Nonetheless, allopolyploidization impacted the evolution of numerous fungal species, including the economically important baker's yeast Saccharomyces cerevisiae (Marcet-Houben & Gabaldón 2015) .
  • The copyright holder for this preprint (which was not this version posted January 17, 2018.
  • V. longisporum is assumed to have largely conserved its allodiploid state as the sizes of its sub-genomes resemble those of haploid Verticillium spp.
  • Nevertheless, not all genes are present in heterozygous copies, as its nuclear ribosomal internal transcribed spacer region is derived only from one of the parents (Inderbitzin et al. 2011b ). certified by peer review) is the author/funder.

Genome analysis

  • Genome assemblies of the two V. longisporum strains (VLB2 and VL20) and V. dahliae strain JR2 were previously published (Faino et al.
  • Telomeric regions were determined based on the telomeric repeat pattern: TAACCC/GGGTTA (minimum three repetitions).
  • Furthermore, additional repeats were identified and characterized using RepeatModeler (v1.0.8).
  • Genome-wide sequence identities between Verticillium strains were calculated with dnadiff (Kurtz et al. 2004 ).
  • Here, only hits with a minimal coverage of 80% with each other were selected.

Gene annotation

  • Verticillium isolates JR2, VLB2 and VL20 were grown for 3 days in potato dextrose broth.
  • Total RNA was extracted based on TRIzol RNA extraction (Simms et al. 1993) .
  • CDNA synthesis, library preparation (TreSep RNA-Seq short-inser library), and Illumina sequencing (single-end 50bp) was performed at the Beijing Genome Institute (BGI, Hong Kong, China).
  • In total, ~2Gb of filtered reads were mapped on the Verticillium genomes using TopHat (Trapnell et al. 2009 ) with Bowtie2 (Langmead & Salzberg 2012) .
  • Predicted genes with internal stop codons were removed from the analysis.

Parental origin determination

  • Certified by peer review) is the author/funder.
  • The copyright holder for this preprint (which was not this version posted January 17, 2018.
  • ; https://doi.org/10.1101/249565 doi: bioRxiv preprint Sub-genomes were divided based on the differences in sequence identities between species A1 and D1 with V. dahliae.
  • Here, only 1-to-1 alignments longer than 10kb and a minimum of 80% identity were retained.
  • Here, hits with a minimum subject and query coverage of 80% were used.

Gene conversion and genomic rearrangements

  • Double copy genes were retrieved by nucleotide BLAST (v2.6.0+) and the sequence identity determined.
  • Here, hits with a minimum subject and query coverage of 80% were used.
  • In order to confirm the breaks in synteny, filtered V. longisporum reads of VLB2 were aligned to the V. longisporum VL20 genome with the Burrows-Wheeler Aligner certified by peer review) is the author/funder.
  • ; https://doi.org/10.1101/249565 doi: bioRxiv preprint (BWA) and further processed with the samtools package (v1.3.1) (Li et al. 2009) .
  • The association between breaks with repeats was tested through permutation.

Phylogenetic tree construction

  • The phylogenetic tree of the nuclear DNA was based on the nucleotide sequences of the ascomycete set BUSCO orthologs present in clade Flavnonexudans Verticillium spp. (Simão et al. 2015) .
  • Nuclear and mitochondrial genomes of Verticillium spp. other than V. longisporum were previously sequenced and assembled (Shi-Kunne et al. forthcoming; Faino et al. 2015; Jelen et al. 2016) .
  • Whole-genome alignments for tree construction were performed by mafft (v7.271) (default settings) (Katoh & Standley 2013; Katoh et al. 2002) , and subsequently the likelihood phylogenetic tree was reconstricted using RAxML with the GTRGAMMA substitution model (v8.2.0) (Stamatakis 2014) . certified by peer review) is the author/funder.
  • ; https://doi.org/10.1101/249565 doi: bioRxiv preprint.

V. longisporum displays a mosaic genome structure

  • The genomes of two V. longisporum strains were analysed to investigate the impact of hybridization on the genome structure.
  • These genome sizes exceed double the amount of the telomere-to-telomere sequenced V. dahliae strains JR2 (36.2 Mb) and VdLs17 (36.0 Mb) (Faino et al. 2015) .
  • The V. longisporum genomes were also screened for telomere-specific repeats (TAACCC/GGGTTA) to estimate the number of chromosomes.
  • In allopolyploid organisms, parental origin determination is elementary to investigate genome evolution in the hybridization aftermath.
  • The copyright holder for this preprint (which was not this version posted January 17, 2018.

Genomic rearrangements are responsible for the mosaic genome

  • Typically, a mosaic structure of a hybrid genome can originate from gene conversion or from chromosomal rearrangements between DNA strands of different parental origin (Mixão & Gabaldón 2018) .
  • To aid gene annotation with the BRAKER1 1.9 pipeline (Hoff et al. 2016 ), ~2 Gb of filtered RNA-seq reads were generated from fungal certified by peer review) is the author/funder.
  • Over 80% of the V. longisporum genes are present in two copies whereas, similar to V. dahliae, almost all genes (97-98%) are present in one copy within each of the V. longisporum sub-genomes.
  • Moreover, of the 7,620 genes that are present in two copies in VLB2 and VL20, only 5 genes were found to be highly identical (<1%, nucleotide sequence identity) in VLB2, whereas the corresponding gene pair in VL20 was more diverse (>1%, nucleotide sequence identity) .
  • The copyright holder for this preprint (which was not this version posted January 17, 2018.

V. longisporum loses heterozygosity through deletions

  • Loss of heterozygosity may occur through gene loss or, alternatively, single-copy genes may originate from parent-specific contributions.
  • As 12% of the singly copy genes in strain VLB2 are present in two copies in strain VL20, and 16% of the single copy genes in VL20 are present in two copies in VLB2, gene deletion seems to be an on-going process in V. longisporum evolution since both strains are derived from the same hybridization event (Depotter et al. 2017b ).

Also the mitochondrial genome has a bi-parental origin

  • To determine how Verticillium species A1 and D1 relate to other species in the clade Flavnonexudans, a phylogenetic tree was constructed based on 1,194 Ascomycota Benchmarking Universal Single-Copy Orthologs that are present in all members of Verticillium clade Flavnonexudans .
  • The copyright holder for this preprint (which was not this version posted January 17, 2018.
  • In addition to genomic DNA, the V. longisporum clade Flavnonexudans phylogeny was also determined based on mitochondrial DNA .
  • The hybrid nature of the V. longisporum mtDNA was furthermore confirmed with a phylogenetic analysis based on a 3.5 kb region that displays 0.7% higher average sequence identity to V. dahliae than to V. nonalfalfae.
  • ; https://doi.org/10.1101/249565 doi: bioRxiv preprint.

DISCUSSION

  • Divergent evolution often fixates genomic incompatibilities between populations, leading to reproductive isolation and eventually even speciation (Seehausen et al. 2014) .
  • Conceivably, extensive genome alterations occurred after hybridization, facilitating the V. longisporum genome to reach a stable equilibrium.
  • Genomic rearrangements often result from double-strand DNA breaks that are erroneously repaired based on templates that display high sequence similarity (Seidl & Thomma 2014) .
  • The copyright holder for this preprint (which was not this version posted January 17, 2018.
  • Mitochondrial DNA is subjected to laws different from the Mendelian principles of segregation and independent assortment as it is maternally inherited in most sexual eukaryotes, including numerous fungal species (Basse 2010) .

Conclusion

  • The V. longisporum genome consists of two near to complete genomes of its haploid parents.
  • The copyright holder for this preprint (which was not this version posted January 17, 2018.
  • The relative difference in GC content (dGC) between genes in double copy, also known as Lane 5.
  • Gene pairs that encountered gene conversion (purple dots in the red zones) have sequence divergence of more than one percent in one V. longisporum strain and less than one percent in the other strain.
  • In other cases, pairs that differ less than one percent are depicted as a black dot, whereas a difference higher than one percent is depicted as a blue dot.

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1
Research Article
1
Nuclear and mitochondrial genomes of the hybrid fungal plant pathogen
2
Verticillium longisporum display a mosaic structure
3
4
Authors: Jasper R.L. Depotter
1,2†
, Fabian van Beveren
1†
, Grardy C.M. van den Berg
1
, Thomas
5
A. Wood
2‡
, Bart P.H.J. Thomma
1*‡
, Michael F. Seidl
1*‡
6
7
1
Laboratory of Phytopathology, Wageningen University, Droevendaalsesteeg 1, 6708 PB
8
Wageningen, The Netherlands
9
2
Department of Crops and Agronomy, National Institute of Agricultural Botany, Huntingdon
10
Road, CB3 0LE Cambridge, United Kingdom
11
12
† These authors contributed equally to this work
13
‡ These authors contributed equally to this work
14
*For correspondence:
15
Bart P.H.J. Thomma, Laboratory of Phytopathology, Wageningen
16
University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands. Tel. 0031-317-
17
484536, e-mail: bart.thomma@wur.nl
18
Michael F. Seidl, Laboratory of Phytopathology, Wageningen
19
University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands. Tel. 0031-317-
20
484536, e-mail: michael.seidl@wur.nl
21
certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was notthis version posted January 17, 2018. ; https://doi.org/10.1101/249565doi: bioRxiv preprint

2
ABSTRACT
22
Allopolyploidization, genome duplication through interspecific hybridization, is an important
23
evolutionary mechanism that can enable organisms to adapt to environmental changes or
24
stresses. This increased adaptive potential of allopolyploids can be particularly relevant for
25
plant pathogens in their quest for host immune response evasion. Allodiploidization likely
26
caused the shift in host range of the fungal pathogen plant Verticillium longisporum, as V.
27
longisporum mainly infects Brassicaceae plants in contrast to haploid Verticillium spp. In this
28
study, we investigated the allodiploid genome structure of V. longisporum and its evolution in
29
the hybridization aftermath. The nuclear genome of V. longisporum displays a mosaic
30
structure, as numerous contigs consists of sections of both parental origins. V. longisporum
31
encountered extensive genome rearrangements, whereas the contribution of gene conversion
32
is negligible. Thus, the mosaic genome structure mainly resulted from genomic
33
rearrangements between parental chromosome sets. Furthermore, a mosaic structure was also
34
found in the mitochondrial genome, demonstrating its bi-parental inheritance. In conclusion,
35
the nuclear and mitochondrial genomes of V. longisporum parents interacted dynamically in
36
the hybridization aftermath. Conceivably, novel combinations of DNA sequence of different
37
parental origin facilitated genome stability after hybridization and consecutive niche
38
adaptation of V. longisporum.
39
40
Key words: whole-genome duplication, allopolyploidy, genomic rearrangement, Verticillium
41
stem striping, Verticillium wilt, Brassica
42
certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was notthis version posted January 17, 2018. ; https://doi.org/10.1101/249565doi: bioRxiv preprint

3
INTRODUCTION
43
Whole-genome duplication (WGD) is an important evolutionary mechanism that facilitates
44
environmental adaptation (Van de Peer et al. 2017; Mallet 2005). The duplication of genomic
45
content increases genomic plasticity, leading to an augmented adaptive potential of organisms
46
that underwent WGD. Consequently, polyploids have been associated with increased
47
invasiveness (te Beest et al. 2012) and resistance to environmental stresses (Lohaus & Van de
48
Peer 2016). For instance, numerous plant species that survived the Cretaceous-Palaeogene
49
mass extinction, 66 million years ago, underwent a WGD which is thought to have
50
contributed to their increased survival rates (Vanneste et al. 2014a; Vanneste et al. 2014b).
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Both genome copies involved in WGD may have the same species origin, i.e.
52
autopolyploidization, or originate from different species as a result of interspecific
53
hybridization, i.e. allopolyploidization. In general, allopolyploids are believed to have a
54
higher adaptive potential than autopolyploids due to the increased genetic divergence between
55
the chromosome sets.
56
The impact of allopolyploidization has mainly been investigated in plants, as
57
approximately a tenth of all plant species consists of allopolyploids (Barker et al. 2015). In
58
contrast, allopolyploidization in fungi is far less intensively investigated (Campbell et al.
59
2016). Nonetheless, allopolyploidization impacted the evolution of numerous fungal species,
60
including the economically important baker’s yeast Saccharomyces cerevisiae (Marcet-
61
Houben & Gabaldón 2015). The increased adaptive potential enabled allopolyploid fungi to
62
develop desirable traits that can be exploited in industrial bioprocessing (Peris et al. 2017).
63
For instance, at least two recent hybridization events between S. cerevisiae and its close
64
relative Saccharomyces eubayanus gave rise to Saccharomyces pastorianus, a species with
65
high cold tolerance and good maltose/maltotriose utilization capabilities, which is exploited in
66
certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was notthis version posted January 17, 2018. ; https://doi.org/10.1101/249565doi: bioRxiv preprint

4
the production of lager beer that requires barley to be malted at low temperatures (Gibson &
67
Liti 2015).
68
Allopolyploid genomes experience a so-called “genome shock” upon hybridization,
69
inciting major genomic reorganizations that can manifest by genome rearrangements,
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extensive gene loss, transposon activation, and alterations in gene expression (Doyle et al.
71
2008). These early stage alterations are primordial for hybrid survival, as divergent evolution
72
is principally associated with incompatibilities between the parental genomes (Matute et al.
73
2010). Allopolyploids benefit from a thorough re-organization where negative interactions
74
between the parental genomes are purged. Frequently, heterozygosity is lost for many regions
75
in the allopolyploid genome (Mixão & Gabaldón 2018). This can be a result of the direct loss
76
of a duplicated gene copy through deletion or gene conversion, a process where one of the
77
copies substitutes its homeologous counterpart (McGrath et al. 2014). Gene conversion and
78
the homogenization of complete chromosomes played a pivotal role in the evolution of the
79
osmotolerant yeast species Pichia sorbitophila (Louis et al. 2012). In total, two of its seven
80
chromosome pairs consist of partly heterozygous, partly homozygous sections, whereas two
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chromosome pairs are completely homozygous. Gene conversion may eventually result in
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chromosomes consisting of sections of both parental origins as “mosaic genomes
83
(Stukenbrock et al. 2012). However, mosaic genomes can also arise through recombination
84
between chromosomes of the different parents, such as in the hybrid yeast
85
Zygosaccharomyces parabailii (Ortiz-Merino et al. 2017).
86
Plant pathogens are often thought to evolve while being engaged in arms races with
87
their hosts; pathogens evolve to evade host immunity while plant hosts attempt to intercept
88
pathogen ingress (Cook et al. 2015). Due to the increased adaptation potential,
89
allopolyploidization has been proposed as a potent driver in pathogen evolution (Depotter et
90
al. 2016b). Allopolyploids often have different pathogenic traits than their parental lineages,
91
certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was notthis version posted January 17, 2018. ; https://doi.org/10.1101/249565doi: bioRxiv preprint

5
such as higher virulence (Husson et al. 2015; Brasier & Kirk 2001) and shifted host ranges
92
(Inderbitzin et al. 2011b; Zeise & Tiedemann 2002). Within the fungal genus Verticillium,
93
allodiploidization resulted in the emergence of a novel pathogen on brassicaceous plants;
94
Verticillium longisporum (Inderbitzin et al. 2011b; Depotter et al. 2017b). Similar to haploid
95
Verticillium spp., V. longisporum is thought to have a predominant asexual reproduction as a
96
sexual cycle has never been described and populations are not outcrossing (Depotter et al.
97
2017b; Short et al. 2014). V. longisporum is sub-divided into three lineages, each representing
98
a separate hybridization event (Inderbitzin et al. 2011b). The economically most important
99
lineage is A1/D1 that originates from hybridization between Verticillium species A1 and D1
100
that have hitherto not been found in their haploid states. V. longisporum lineage A1/D1 is the
101
main causal agent of Verticillium stem striping on oilseed rape (Novakazi et al. 2015) and its
102
economic importance as emerging pathogen is increasing worldwide (Depotter et al. 2017a).
103
A recent study revealed that lineage A1/D1 can be further divided into two genetically distinct
104
populations, which have been named ‘A1/D1 Westand ‘A1/D1 East’ after their geographic
105
occurrence in Europe (Depotter et al. 2017b). Nevertheless, both populations were shown to
106
originate the same hybridization event (Depotter et al. 2017b).
107
V. longisporum is assumed to have largely conserved its allodiploid state as the sizes
108
of its sub-genomes resemble those of haploid Verticillium spp. (Depotter et al. 2017b; Shi-
109
Kunne et al. forthcoming; Fogelqvist et al. 2018). Nevertheless, not all genes are present in
110
heterozygous copies, as its nuclear ribosomal internal transcribed spacer region is derived
111
only from one of the parents (Inderbitzin et al. 2011b). Here, we investigated the evolution of
112
the allodiploid genome of V. longisporum and determined to what extent heterozygosity is
113
lost.
114
certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.
The copyright holder for this preprint (which was notthis version posted January 17, 2018. ; https://doi.org/10.1101/249565doi: bioRxiv preprint

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  • ...When phylogenetic comparisons between mitochondrial and nuclear data sets in fungi differ, hybridization, introgression or incomplete lineage sorting among other events could explain incongruences (Depotter et al. 2018; Giordano et al. 2018)....

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  • ...New fungal hybrids are reported on a regular basis (Depotter et al., 2018; Giordano et al., 2018)....

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  • ...Comparisons between nuclear and mitochondrial genomes are useful to identify hybridization, introgression or incomplete lineage sorting among other evolutionary events (Depotter et al., 2018; Gonthier et al., 2018)....

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Abstract: Fungal mitochondrial genomes encode for genes involved in crucial cellular processes, such as oxidative phosphorylation and mitochondrial translation, and these genes have been used as molecular markers for population genetics studies. Coccidioides immitis and C. posadasii are endemic fungal pathogens that cause coccidioidomycosis in arid regions across both American continents. To date, almost one hundred Coccidioides strains have been sequenced. The focus of these studies has been exclusively to infer patterns of variation of nuclear genomes (nucDNA). However, their mitochondrial genomes (mtDNA) have not been studied. In this report, we describe the assembly and annotation of mitochondrial reference genomes for two representative strains of C. posadasii and C. immitis, as well as assess population variation among 77 published genomes. The circular-mapping mtDNA molecules are 68.2 Kb in C. immitis and 75.1 Kb in C. posadasii. We identified the fourteen mitochondrial protein-coding genes common to most fungal mitochondria, including genes encoding the small and large ribosomal RNAs (rns and rnl), the RNA subunit of RNAse P (rnpB), and 26 tRNAs organized in polycistronic transcription units, which are mostly syntenic across different populations and species of Coccidioides. Both Coccidioides species are characterized by a large number of group I and II introns, harboring twice the number of elements as compared to closely related Onygenales. The introns contain complete or truncated ORFs with high similarity to homing endonucleases of the LAGLIDADG and GIY-YIG families. Phylogenetic comparison of the mtDNA and nucDNA genomes shows discordance, possibly due to differences in patterns of inheritance. In summary, this work represents the first complete assessment of mitochondrial genomes among several isolates of both species of Coccidioides, and provides a foundation for future functional work.

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01 May 2014-Bioinformatics
TL;DR: This work presents some of the most notable new features and extensions of RAxML, such as a substantial extension of substitution models and supported data types, the introduction of SSE3, AVX and AVX2 vector intrinsics, techniques for reducing the memory requirements of the code and a plethora of operations for conducting post-analyses on sets of trees.
Abstract: Motivation: Phylogenies are increasingly used in all fields of medical and biological research. Moreover, because of the next-generation sequencing revolution, datasets used for conducting phylogenetic analyses grow at an unprecedented pace. RAxML (Randomized Axelerated Maximum Likelihood) is a popular program for phylogenetic analyses of large datasets under maximum likelihood. Since the last RAxML paper in 2006, it has been continuously maintained and extended to accommodate the increasingly growing input datasets and to serve the needs of the user community. Results: I present some of the most notable new features and extensions of RAxML, such as a substantial extension of substitution models and supported data types, the introduction of SSE3, AVX and AVX2 vector intrinsics, techniques for reducing the memory requirements of the code and a plethora of operations for conducting postanalyses on sets of trees. In addition, an up-to-date 50-page user manual covering all new RAxML options is available. Availability and implementation: The code is available under GNU

18,576 citations


Additional excerpts

  • ...2.0) (Stamatakis 2014)....

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Journal ArticleDOI
Aaron R. Quinlan1, Ira M. Hall1Institutions (1)
15 Mar 2010-Bioinformatics
TL;DR: A new software suite for the comparison, manipulation and annotation of genomic features in Browser Extensible Data (BED) and General Feature Format (GFF) format, which allows the user to compare large datasets (e.g. next-generation sequencing data) with both public and custom genome annotation tracks.
Abstract: Motivation: Testing for correlations between different sets of genomic features is a fundamental task in genomics research. However, searching for overlaps between features with existing webbased methods is complicated by the massive datasets that are routinely produced with current sequencing technologies. Fast and flexible tools are therefore required to ask complex questions of these data in an efficient manner. Results: This article introduces a new software suite for the comparison, manipulation and annotation of genomic features in Browser Extensible Data (BED) and General Feature Format (GFF) format. BEDTools also supports the comparison of sequence alignments in BAM format to both BED and GFF features. The tools are extremely efficient and allow the user to compare large datasets (e.g. next-generation sequencing data) with both public and custom genome annotation tracks. BEDTools can be combined with one another as well as with standard UNIX commands, thus facilitating routine genomics tasks as well as pipelines that can quickly answer intricate questions of large genomic datasets. Availability and implementation: BEDTools was written in C++. Source code and a comprehensive user manual are freely available at http://code.google.com/p/bedtools

14,088 citations


"Nuclear and mitochondrial genomes o..." refers background in this paper

  • ...26.0) to calculate the significance of the break/repeat association (Quinlan & Hall 2010)....

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