A comparative analysis of planarian genomes reveals regulatory conservation in the face of rapid structural divergence.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
19 Sep 2024
19 Sep 2024
Historique:
received:
20
01
2024
accepted:
30
08
2024
medline:
19
9
2024
pubmed:
19
9
2024
entrez:
18
9
2024
Statut:
epublish
Résumé
The planarian Schmidtea mediterranea is being studied as a model species for regeneration, but the assembly of planarian genomes remains challenging. Here, we report a high-quality haplotype-phased, chromosome-scale genome assembly of the sexual S2 strain of S. mediterranea and high-quality chromosome-scale assemblies of its three close relatives, S. polychroa, S. nova, and S. lugubris. Using hybrid gene annotations and optimized ATAC-seq and ChIP-seq protocols for regulatory element annotation, we provide valuable genome resources for the planarian research community and a first comparative perspective on planarian genome evolution. Our analyses reveal substantial divergence in protein-coding sequences and regulatory regions but considerable conservation within promoter and enhancer annotations. We also find frequent retrotransposon-associated chromosomal inversions and interchromosomal translocations within the genus Schmidtea and, remarkably, independent and nearly complete losses of ancestral metazoan synteny in Schmidtea and two other flatworm groups. Overall, our results suggest that platyhelminth genomes can evolve without syntenic constraints.
Identifiants
pubmed: 39294119
doi: 10.1038/s41467-024-52380-9
pii: 10.1038/s41467-024-52380-9
doi:
Substances chimiques
Retroelements
0
Types de publication
Journal Article
Comparative Study
Langues
eng
Sous-ensembles de citation
IM
Pagination
8215Informations de copyright
© 2024. The Author(s).
Références
Kon, T. et al. The genetic basis of morphological diversity in domesticated goldfish. Curr. Biol. 30, 2260–2274.e6 (2020).
pubmed: 32392470
doi: 10.1016/j.cub.2020.04.034
Gordon, C. T. et al. De novo mutations in SMCHD1 cause Bosma arhinia microphthalmia syndrome and abrogate nasal development. Nat. Genet. 49, 249–255 (2017).
pubmed: 28067911
doi: 10.1038/ng.3765
King, M.-C. & Wilson, A. C. Evolution at two levels in humans and chimpanzees: Their macromolecules are so alike that regulatory mutations may account for their biological differences. Science 188, 107–116 (1975).
pubmed: 1090005
doi: 10.1126/science.1090005
Roscito, J. G. et al. Phenotype loss is associated with widespread divergence of the gene regulatory landscape in evolution. Nat. Commun. 9, 4737 (2018).
pubmed: 30413698
pmcid: 6226452
doi: 10.1038/s41467-018-07122-z
Kvon, E. Z. et al. Progressive loss of function in a limb enhancer during snake evolution. Cell 167, 633–642.e11 (2016).
pubmed: 27768887
pmcid: 5484524
doi: 10.1016/j.cell.2016.09.028
Osipova, E. et al. Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds. Science 379, 185–190 (2023).
pubmed: 36634192
doi: 10.1126/science.abn7050
Bontempo, M. & Luiza, A. Gene losses in the common vampire bat illuminate molecular adaptations to blood feeding. Sci. Adv. 8, eabm6494 (2022).
Simakov, O. et al. Deeply conserved synteny and the evolution of metazoan chromosomes. Sci. Adv. 8, eabi5884 (2022).
pubmed: 35108053
pmcid: 8809688
doi: 10.1126/sciadv.abi5884
Wang, S. et al. Scallop genome provides insights into evolution of bilaterian karyotype and development. Nat. Ecol. Evol. 1, 0120 (2017).
pubmed: 28812685
pmcid: 10970998
doi: 10.1038/s41559-017-0120
Schultz, D. T. et al. Ancient gene linkages support ctenophores as sister to other animals. Nature 1–8 (2023) https://doi.org/10.1038/s41586-023-05936-6 .
Bhutkar, A. et al. Chromosomal rearrangement inferred from comparisons of 12 Drosophila genomes. Genetics 179, 1657–1680 (2008).
pubmed: 18622036
pmcid: 2475759
doi: 10.1534/genetics.107.086108
Tandonnet, S. et al. Chromosome-wide evolution and sex determination in the three-sexed nematode Auanema rhodensis. G3 GenesGenomesGenetics 9, 1211–1230 (2019).
doi: 10.1534/g3.119.0011
Rowley, M. J. & Corces, V. G. Organizational principles of 3D genome architecture. Nat. Rev. Genet. 19, 789–800 (2018).
pubmed: 30367165
doi: 10.1038/s41576-018-0060-8
Rao, S. S. P. et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665–1680 (2014).
pubmed: 25497547
pmcid: 5635824
doi: 10.1016/j.cell.2014.11.021
Lupiáñez, D. G. et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161, 1012–1025 (2015).
pubmed: 25959774
pmcid: 4791538
doi: 10.1016/j.cell.2015.04.004
Franke, M. et al. Formation of new chromatin domains determines pathogenicity of genomic duplications. Nature 538, 265–269 (2016).
pubmed: 27706140
doi: 10.1038/nature19800
Alekseyenko, A. A. et al. The oncogenic BRD4-NUT chromatin regulator drives aberrant transcription within large topological domains. Genes Dev. 29, 1507–1523 (2015).
pubmed: 26220994
pmcid: 4526735
doi: 10.1101/gad.267583.115
Akdemir, K. C. et al. Disruption of chromatin folding domains by somatic genomic rearrangements in human cancer. Nat. Genet. 52, 294–305 (2020).
pubmed: 32024999
pmcid: 7058537
doi: 10.1038/s41588-019-0564-y
Acemel, R. D. et al. A single three-dimensional chromatin compartment in amphioxus indicates a stepwise evolution of vertebrate Hox bimodal regulation. Nat. Genet. 48, 336–341 (2016).
pubmed: 26829752
doi: 10.1038/ng.3497
Letelier, J. et al. Evolutionary emergence of the rac3b / rfng / sgca regulatory cluster refined mechanisms for hindbrain boundaries formation. Proc. Natl. Acad. Sci. 115, (2018).
Luo, X. et al. 3D Genome of macaque fetal brain reveals evolutionary innovations during primate corticogenesis. Cell 184, 723–740.e21 (2021).
pubmed: 33508230
doi: 10.1016/j.cell.2021.01.001
Hoencamp, C. et al. 3D genomics across the tree of life reveals condensin II as a determinant of architecture type. Science 372, 984–989 (2021).
pubmed: 34045355
pmcid: 8172041
doi: 10.1126/science.abe2218
Ivankovic, M. et al. Model systems for regeneration: planarians. Development 146, dev167684 (2019).
pubmed: 31511248
doi: 10.1242/dev.167684
Reddien, P. W. The cellular and molecular basis for planarian regeneration. Cell 175, 327–345 (2018).
pubmed: 30290140
pmcid: 7706840
doi: 10.1016/j.cell.2018.09.021
Robb, S. M. C., Gotting, K., Ross, E. & Sánchez Alvarado, A. SmedGD 2.0: The Schmidtea mediterranea genome database. Genesis 53, 535–546 (2015).
pubmed: 26138588
pmcid: 4867232
doi: 10.1002/dvg.22872
Grohme, M. A. et al. The genome of Schmidtea mediterranea and the evolution of core cellular mechanisms. Nature 554, 56–61 (2018).
pubmed: 29364871
pmcid: 5797480
doi: 10.1038/nature25473
Guo, L. et al. Island-specific evolution of a sex-primed autosome in a sexual planarian. Nature 606, 329–334 (2022).
pubmed: 35650439
pmcid: 9177419
doi: 10.1038/s41586-022-04757-3
Guo, L., Zhang, S., Rubinstein, B., Ross, E. & Alvarado, A. S. Widespread maintenance of genome heterozygosity in Schmidtea mediterranea. Nat. Ecol. Evol. 1, 1–10 (2016).
doi: 10.1038/s41559-016-0019
Tian, Q. et al. Whole-genome sequence of the planarian Dugesia japonica combining Illumina and PacBio data. Genomics 114, 110293 (2022).
pubmed: 35139429
doi: 10.1016/j.ygeno.2022.110293
Póti, Á., Szüts, D. & Vermezovic, J. Mutational profile of the regenerative process and de novo genome assembly of the planarian Schmidtea polychroa. Nucleic Acids Res. gkad1250 (2024) https://doi.org/10.1093/nar/gkad1250 .
An, Y. et al. Draft genome of Dugesia japonica provides insights into conserved regulatory elements of the brain restriction gene nou-darake in planarians. Zool. Lett. 4, 24 (2018).
doi: 10.1186/s40851-018-0102-2
Duncan, E. M., Chitsazan, A. D., Seidel, C. W. & Sánchez Alvarado, A. Set1 and MLL1/2 target distinct sets of functionally different genomic loci in vivo. Cell Rep. 13, 2741–2755 (2015).
pubmed: 26711341
pmcid: 4707048
doi: 10.1016/j.celrep.2015.11.059
Dattani, A. et al. Epigenetic analyses of planarian stem cells demonstrate conservation of bivalent histone modifications in animal stem cells. Genome Res. 28, 1543–1554 (2018).
pubmed: 30143598
pmcid: 6169894
doi: 10.1101/gr.239848.118
Mihaylova, Y. et al. Conservation of epigenetic regulation by the MLL3/4 tumour suppressor in planarian pluripotent stem cells. Nat. Commun. 9, 3633 (2018).
Gehrke, A. R. et al. Acoel genome reveals the regulatory landscape of whole-body regeneration. Science 363, eaau6173 (2019).
pubmed: 30872491
doi: 10.1126/science.aau6173
Li, D., Taylor, D. H. & Van Wolfswinkel, J. C. PIWI-mediated control of tissue-specific transposons is essential for somatic cell differentiation. Cell Rep. 37, 109776 (2021).
pubmed: 34610311
pmcid: 8532177
doi: 10.1016/j.celrep.2021.109776
Verma, P., Waterbury, C. K. M. & Duncan, E. M. Set1 targets genes with essential identity and tumor-suppressing functions in planarian stem cells. Genes 12, 1182 (2021).
Neiro, J., Sridhar, D., Dattani, A. & Aboobaker, A. Identification of putative enhancer-like elements predicts regulatory networks active in planarian adult stem cells. eLife 11, e79675 (2022).
pubmed: 35997250
pmcid: 9522251
doi: 10.7554/eLife.79675
Pascual-Carreras, E. et al. Wnt/β-catenin signalling is required for pole-specific chromatin remodeling during planarian regeneration. Nat. Commun. 14, 298 (2023).
pubmed: 36653403
pmcid: 9849279
doi: 10.1038/s41467-023-35937-y
Poulet, A., Kratkiewicz, A. J., Li, D. & van Wolfswinkel, J. C. Chromatin analysis of adult pluripotent stem cells reveals a unique stemness maintenance strategy. Sci. Adv. 9, eadh4887 (2023).
pubmed: 37801496
pmcid: 10558129
doi: 10.1126/sciadv.adh4887
Vila-Farré, M. et al. Evolutionary dynamics of whole-body regeneration across planarian flatworms. Nat. Ecol. Evol. 1–17 (2023) https://doi.org/10.1038/s41559-023-02221-7 .
Rozanski, A. et al. PlanMine 3.0—improvements to a mineable resource of flatworm biology and biodiversity. Nucleic Acids Res. 47, D812–D820 (2019).
pubmed: 30496475
doi: 10.1093/nar/gky1070
Lakshmanan, V. et al. Genome-wide analysis of polyadenylation events in Schmidtea mediterranea. G3 GenesGenomesGenetics 6, 3035–3048 (2016).
doi: 10.1534/g3.116.031120
Blythe, M. J. et al. A dual platform approach to transcript discovery for the planarian Schmidtea mediterranea to establish RNAseq for stem cell and regeneration biology. PLOS ONE 5, e15617 (2010).
pubmed: 21179477
pmcid: 3001875
doi: 10.1371/journal.pone.0015617
García-Castro, H. et al. ACME dissociation: a versatile cell fixation-dissociation method for single-cell transcriptomics. Genome Biol. 22, 89 (2021).
pubmed: 33827654
pmcid: 8028764
doi: 10.1186/s13059-021-02302-5
Corces, M. R. et al. An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues. Nat. Methods 14, 959–962 (2017).
pubmed: 28846090
pmcid: 5623106
doi: 10.1038/nmeth.4396
Yan, F., Powell, D. R., Curtis, D. J. & Wong, N. C. From reads to insight: a hitchhiker’s guide to ATAC-seq data analysis. Genome Biol. 21, 22 (2020).
pubmed: 32014034
pmcid: 6996192
doi: 10.1186/s13059-020-1929-3
Shlyueva, D., Stampfel, G. & Stark, A. Transcriptional enhancers: from properties to genome-wide predictions. Nat. Rev. Genet. 15, 272–286 (2014).
pubmed: 24614317
doi: 10.1038/nrg3682
Santos-Rosa, H. et al. Active genes are tri-methylated at K4 of histone H3. Nature 419, 407–411 (2002).
pubmed: 12353038
doi: 10.1038/nature01080
Creyghton, M. P. et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl Acad. Sci. 107, 21931–21936 (2010).
pubmed: 21106759
pmcid: 3003124
doi: 10.1073/pnas.1016071107
Visel, A., Bristow, J. & Pennacchio, L. A. Enhancer identification through comparative genomics. Semin. Cell Dev. Biol. 18, 140–152 (2007).
pubmed: 17276707
pmcid: 1855162
doi: 10.1016/j.semcdb.2006.12.014
Egger, B. et al. A Transcriptomic-Phylogenomic analysis of the evolutionary relationships of flatworms. Curr. Biol. 25, 1347–1353 (2015).
pubmed: 25866392
pmcid: 4446793
doi: 10.1016/j.cub.2015.03.034
Laumer, C. E., Hejnol, A. & Giribet, G. Nuclear genomic signals of the ‘microturbellarian’ roots of Platyhelminth evolutionary innovation. eLife 4, e05503 (2015).
pubmed: 25764302
pmcid: 4398949
doi: 10.7554/eLife.05503
Martín-Durán, J. M., Ryan, J. F., Vellutini, B. C., Pang, K. & Hejnol, A. Increased taxon sampling reveals thousands of hidden orthologs in flatworms. Genome Res. 27, 1263–1272 (2017).
pubmed: 28400424
pmcid: 5495077
doi: 10.1101/gr.216226.116
Brand, J. N., Viktorin, G., Wiberg, R. A. W., Beisel, C. & Schärer, L. Large-scale phylogenomics of the genus Macrostomum (Platyhelminthes) reveals cryptic diversity and novel sexual traits. Mol. Phylogenet. Evol. 166, 107296 (2022).
pubmed: 34438051
doi: 10.1016/j.ympev.2021.107296
Benazzi, M., Puccinelli, I. & Papa, R. D. The planarians of the Dugesia lugubris-polychroa group: taxonomic inferences based on cytogenetic and morphologic data. Accad. Natl Dei Lincei Ser. VIII 48, 369–376 (1970).
Benazzi, M., Baguná, J., Ballester, R., Puccinelli, I. & Papa, R. D. Further contribution to the taxonomy of the «Dugesia lugubris-polychroa Group» with description of Dugesia mediterranea n.sp. (tricladida, paludicola). Bolletino Zool. 42, 81–89 (1975).
doi: 10.1080/11250007509430132
Benazzi, M. & Puccinelli, I. A Robertsonian translocation in the fresh-water triclad Dugesia lugubris: Karyometric analysis and evolutionary inferences. Chromosoma 40, 193–198 (1972).
doi: 10.1007/BF00321464
Leria, L., Sluys, R. & Riutort, M. Diversification and biogeographic history of the Western Palearctic freshwater flatworm genus Schmidtea (Tricladida: Dugesiidae), with a redescription of Schmidtea nova. J. Zool. Syst. Evol. Res. 56, 335–351 (2018).
doi: 10.1111/jzs.12214
Kirilenko, B. M. et al. Integrating gene annotation with orthology inference at scale. Science 380, eabn3107 (2023).
pubmed: 37104600
pmcid: 10193443
doi: 10.1126/science.abn3107
Cebrià, F. et al. FGFR-related gene nou-darake restricts brain tissues to the head region of planarians. Nature 419, 620–624 (2002).
pubmed: 12374980
doi: 10.1038/nature01042
Gurley, K. A., Rink, J. C. & Alvarado, A. S. β-Catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 319, 323–327 (2008).
pubmed: 18063757
doi: 10.1126/science.1150029
Lovell, J. T. et al. GENESPACE tracks regions of interest and gene copy number variation across multiple genomes. eLife 11, e78526 (2022).
pubmed: 36083267
pmcid: 9462846
doi: 10.7554/eLife.78526
Startek, M. et al. Genome-wide analyses of LINE–LINE-mediated nonallelic homologous recombination. Nucleic Acids Res. 43, 2188–2198 (2015).
pubmed: 25613453
pmcid: 4344489
doi: 10.1093/nar/gku1394
Nowotarski, S. H. et al. Planarian Anatomy Ontology: a resource to connect data within and across experimental platforms. Development 148, dev196097 (2021).
Davies, E. L. et al. Embryonic origin of adult stem cells required for tissue homeostasis and regeneration. eLife 6, 4756–4769 (2017).
Fincher, C. T., Wurtzel, O., de Hoog, T., Kravarik, K. M. & Reddien, P. W. Cell type transcriptome atlas for the planarian Schmidtea mediterranea. Science 360, eaaq1736 (2018).
pubmed: 29674431
pmcid: 6563842
doi: 10.1126/science.aaq1736
Plass, M. et al. Cell type atlas and lineage tree of a whole complex animal by single-cell transcriptomics. Science 360, eaaq1723 (2018).
Baguñà, J. et al. From morphology and karyology to molecules. New methods for taxonomical identification of asexual populations of freshwater planarians. A tribute to Professor Mario Benazzi. Ital. J. Zool. 66, 207–214 (1999).
doi: 10.1080/11250009909356258
Hill, J. et al. Unprecedented reorganization of holocentric chromosomes provides insights into the enigma of Lepidopteran chromosome evolution. Sci. Adv. 5, eaau3648 (2019).
pubmed: 31206013
pmcid: 6561736
doi: 10.1126/sciadv.aau3648
Hofstatter, P. G. et al. Repeat-based holocentromeres influence genome architecture and karyotype evolution. Cell 185, 3153–3168.e18 (2022).
pubmed: 35926507
doi: 10.1016/j.cell.2022.06.045
Tsai, I. J. et al. The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496, 57–63 (2013).
pubmed: 23485966
pmcid: 3964345
doi: 10.1038/nature12031
The Evolution of Parasitism: A Phylogenetic Perspective. (Academic Press, San Diego, 2003).
Coghlan, A. et al. Comparative genomics of the major parasitic worms. Nat. Genet. 51, 163–174 (2019).
doi: 10.1038/s41588-018-0262-1
Simakov, O. et al. Deeply conserved synteny resolves early events in vertebrate evolution. Nat. Ecol. Evol. 4, 820–830 (2020).
pubmed: 32313176
pmcid: 7269912
doi: 10.1038/s41559-020-1156-z
Zimmermann, B. et al. Topological structures and syntenic conservation in sea anemone genomes. Nat. Commun. 14, 8270 (2023).
pubmed: 38092765
pmcid: 10719294
doi: 10.1038/s41467-023-44080-7
Liao, I. J.-Y., Lu, T.-M., Chen, M.-E. & Luo, Y.-J. Spiralian genomics and the evolution of animal genome architecture. Brief. Funct. Genomics elad029 (2023) https://doi.org/10.1093/bfgp/elad029 .
Sawh, A. N. & Mango, S. E. Chromosome organization in 4D: insights from C. elegans development. Curr. Opin. Genet. Dev. 75, 101939 (2022).
pubmed: 35759905
doi: 10.1016/j.gde.2022.101939
Crane, E. et al. Condensin-driven remodelling of X chromosome topology during dosage compensation. Nature 523, 240–244 (2015).
pubmed: 26030525
pmcid: 4498965
doi: 10.1038/nature14450
Plessy, C. et al. Extreme Genome Scrambling in Cryptic Oikopleura Dioica Species. (2023) https://doi.org/10.1101/2023.05.09.539028 .
Salvetti, A. et al. Adult stem cell plasticity: Neoblast repopulation in non-lethally irradiated planarians. Dev. Biol. 328, 305–314 (2009).
pubmed: 19389358
doi: 10.1016/j.ydbio.2009.01.029
De Mulder, K. et al. Potential of Macrostomum lignano to recover from γ-ray irradiation. Cell Tissue Res 339, 527–542 (2010).
pubmed: 20127258
pmcid: 2831187
doi: 10.1007/s00441-009-0915-6
Collins III, J. J. et al. Adult somatic stem cells in the human parasite Schistosoma mansoni. Nature 494, 476–479 (2013).
doi: 10.1038/nature11924
Koziol, U., Rauschendorfer, T., Zanon Rodríguez, L., Krohne, G. & Brehm, K. The unique stem cell system of the immortal larva of the human parasite Echinococcus multilocularis. EvoDevo 5, 10 (2014).
pubmed: 24602211
pmcid: 4015340
doi: 10.1186/2041-9139-5-10
Richardson, C. & Jasin, M. Coupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells. Mol. Cell. Biol. 20, 9068–9075 (2000).
pubmed: 11074004
pmcid: 86559
doi: 10.1128/MCB.20.23.9068-9075.2000
Boboila, C. et al. Alternative end-joining catalyzes robust IgH locus deletions and translocations in the combined absence of ligase 4 and Ku70. Proc. Natl Acad. Sci. USA. 107, 3034–3039 (2010).
pubmed: 20133803
pmcid: 2840344
doi: 10.1073/pnas.0915067107
Ramsden, D. A. & Nussenzweig, A. Mechanisms driving chromosomal translocations: Lost in time and space. Oncogene 40, 4263–4270 (2021).
pubmed: 34103687
pmcid: 8238880
doi: 10.1038/s41388-021-01856-9
Howe, J., Rink, J. C., Wang, B. & Griffin, A. S. Multicellularity in animals: The potential for within-organism conflict. Proc. Natl Acad. Sci. 119, e2120457119 (2022).
pubmed: 35862435
pmcid: 9371690
doi: 10.1073/pnas.2120457119
Merryman, M. S., Alvarado, A. S. & Jenkin, J. C. Culturing planarians in the laboratory. in Planarian regeneration: Methods and protocols 241–258 (Springer New York, New York, NY, 2018).
Cohen, S. S. & Lichtenstein, J. The isolation of deoxyribonucleic acid from bacterial extracts by precipitation with streptomycin. J. Biol. Chem. 235, PC55–PC56 (1960).
pubmed: 13694444
doi: 10.1016/S0021-9258(20)81364-7
Oxenburgh, M. S. & Snoswell, A. M. Use of Streptomycin in the Separation of Nucleic Acids from Protein in a Bacterial Extract. Nature 207, 1416–1417 (1965).
pubmed: 5886058
doi: 10.1038/2071416a0
Deguchi, T., Ishi, A. & Tanaka, M. Binding of aminoglycoside antibiotics to acidic mucopolysaccharides. J. Antibiot. 31, 150–155 (1978)..
Lis, J. T. & Schleif, R. Size fractionation of double-stranded DNA by precipitation with polyethylene glycol. Nucleic Acids Res. 2, 383–389 (1975).
pubmed: 236548
pmcid: 342844
doi: 10.1093/nar/2.3.383
Cheng, H., Concepcion, G. T., Feng, X., Zhang, H. & Li, H. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat. Methods 18, 170–175 (2021).
pubmed: 33526886
pmcid: 7961889
doi: 10.1038/s41592-020-01056-5
Ghurye, J., Pop, M., Koren, S., Bickhart, D. & Chin, C.-S. Scaffolding of long read assemblies using long range contact information. BMC Genomics 18, 527 (2017).
pubmed: 28701198
pmcid: 5508778
doi: 10.1186/s12864-017-3879-z
Li, H. New strategies to improve minimap2 alignment accuracy. Bioinformatics 37, 4572–4574 (2021).
pubmed: 34623391
pmcid: 8652018
doi: 10.1093/bioinformatics/btab705
Goel, M., Sun, H., Jiao, W.-B. & Schneeberger, K. SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies. Genome Biol. 20, 277 (2019).
pubmed: 31842948
pmcid: 6913012
doi: 10.1186/s13059-019-1911-0
Poplin, R. et al. A universal SNP and small-indel variant caller using deep neural networks. Nat. Biotechnol. 36, 983–987 (2018).
pubmed: 30247488
doi: 10.1038/nbt.4235
Ou, S. et al. Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol. 20, 275 (2019).
pubmed: 31843001
pmcid: 6913007
doi: 10.1186/s13059-019-1905-y
Neumann, P., Novák, P., Hoštáková, N. & Macas, J. Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mob. DNA 10, 1 (2019).
pubmed: 30622655
pmcid: 6317226
doi: 10.1186/s13100-018-0144-1
Novák, P., Neumann, P. & Macas, J. Global analysis of repetitive DNA from unassembled sequence reads using RepeatExplorer2. Nat. Protoc. 15, 3745–3776 (2020).
pubmed: 33097925
doi: 10.1038/s41596-020-0400-y
Kearse, M. et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).
pubmed: 22543367
pmcid: 3371832
doi: 10.1093/bioinformatics/bts199
Zhang, Y., Chu, J., Cheng, H. & Li, H. De novo reconstruction of satellite repeat units from sequence data. ArXiv arXiv:2304.09729v1 (2023).
Kokot, M., Długosz, M. & Deorowicz, S. KMC 3: counting and manipulating k -mer statistics. Bioinformatics 33, 2759–2761 (2017).
pubmed: 28472236
doi: 10.1093/bioinformatics/btx304
Liu, S.-Y. & Rink, J. C. Total RNA Isolation from Planarian Tissues. 1774 (Humana Press, New York, NY, 2018).
Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37, 907–915 (2019).
pubmed: 31375807
pmcid: 7605509
doi: 10.1038/s41587-019-0201-4
Kovaka, S. et al. Transcriptome assembly from long-read RNA-seq alignments with StringTie2. Genome Biol. 20, 278 (2019).
pubmed: 31842956
pmcid: 6912988
doi: 10.1186/s13059-019-1910-1
Tang, A. D. et al. Full-length transcript characterization of SF3B1 mutation in chronic lymphocytic leukemia reveals downregulation of retained introns. Nat. Commun. 11, 1438 (2020).
pubmed: 32188845
pmcid: 7080807
doi: 10.1038/s41467-020-15171-6
Gleeson, J. et al. Accurate expression quantification from nanopore direct RNA sequencing with NanoCount. Nucleic Acids Res 50, e19 (2022).
pubmed: 34850115
doi: 10.1093/nar/gkab1129
Buenrostro, J. D., Wu, B., Chang, H. Y. & Greenleaf, W. J. ATAC-seq: A method for assaying chromatin accessibility genome-wide. Curr. Protoc. Mol. Biol. 109, 21.29.1–21.29.9 (2015).
pubmed: 25559105
doi: 10.1002/0471142727.mb2129s109
Zhang, Y. et al. Model-based Analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
pubmed: 18798982
pmcid: 2592715
doi: 10.1186/gb-2008-9-9-r137
Crusoe, M. R. et al. The khmer software package: enabling efficient nucleotide sequence analysis. F1000Res. 4, 900 (2015).
Yu, G., Wang, L.-G. & He, Q.-Y. ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics 31, 2382–2383 (2015).
pubmed: 25765347
doi: 10.1093/bioinformatics/btv145
Ramírez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res 44, W160–W165 (2016).
pubmed: 27079975
pmcid: 4987876
doi: 10.1093/nar/gkw257
Kurtenbach, S. & Harbour, J. W. SparK: A publication-quality NGS visualization tool. Preprint at https://doi.org/10.1101/845529 (2019).
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278
pmcid: 2832824
doi: 10.1093/bioinformatics/btq033
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886
doi: 10.1093/bioinformatics/bts635
Ou, J. et al. ATACseqQC: a Bioconductor package for post-alignment quality assessment of ATAC-seq data. BMC Genomics 19, 169 (2018).
pubmed: 29490630
pmcid: 5831847
doi: 10.1186/s12864-018-4559-3
Newell, R. et al. ChIP-R: Assembling reproducible sets of ChIP-seq and ATAC-seq peaks from multiple replicates. Genomics 113, 1855–1866 (2021).
pubmed: 33878366
doi: 10.1016/j.ygeno.2021.04.026
Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238 (2019).
pubmed: 31727128
pmcid: 6857279
doi: 10.1186/s13059-019-1832-y
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., Haeseler, Avon & Jermiin, L. S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).
pubmed: 28481363
pmcid: 5453245
doi: 10.1038/nmeth.4285
Minh, B. Q. et al. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).
pubmed: 32011700
pmcid: 7182206
doi: 10.1093/molbev/msaa015
Armstrong, J. et al. Progressive Cactus is a multiple-genome aligner for the thousand-genome era. Nature 587, 246–251 (2020).
pubmed: 33177663
pmcid: 7673649
doi: 10.1038/s41586-020-2871-y
Zhang, X., Kaplow, I. M., Wirthlin, M., Park, T. Y. & Pfenning, A. R. HALPER facilitates the identification of regulatory element orthologs across species. Bioinformatics 36, 4339–4340 (2020).
pubmed: 32407523
pmcid: 7520040
doi: 10.1093/bioinformatics/btaa493
Hickey, G., Paten, B., Earl, D., Zerbino, D. & Haussler, D. HAL: a hierarchical format for storing and analyzing multiple genome alignments. Bioinformatics 29, 1341–1342 (2013).
pubmed: 23505295
pmcid: 3654707
doi: 10.1093/bioinformatics/btt128
Wang, Y. et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49 (2012).
pubmed: 22217600
pmcid: 3326336
doi: 10.1093/nar/gkr1293
Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).
pubmed: 26059717
doi: 10.1093/bioinformatics/btv351