Gapless genome assembly of Colletotrichum higginsianum reveals chromosome structure and association of transposable elements with secondary metabolite gene clusters

Detalhes bibliográficos
Autor(a) principal: Dallery, Jean-Félix
Data de Publicação: 2017
Outros Autores: Lapalu, Nicolas, Zampounis, Antonios, Pigné, Sandrine, Luyten, Isabelle, Amselem, Joëlle, Wittenberg, Alexander H. J., Zhou, Shiguo, Queiroz, Marisa V. de, Robin, Guillaume P., Auger, Annie, Hainaut, Matthieu, Henrissat, Bernard, Kim, Ki-Tae, Lee, Yong-Hwan, Lespinet, Olivier, Schwartz, David C., Thon, Michael R., Richard J. O’Connell
Tipo de documento: Artigo
Idioma: eng
Título da fonte: LOCUS Repositório Institucional da UFV
Texto Completo: https://www.ncbi.nlm.nih.gov/pubmed/28851275
http://www.locus.ufv.br/handle/123456789/13887
Resumo: The ascomycete fungus Colletotrichum higginsianum causes anthracnose disease of brassica crops and the model plant Arabidopsis thaliana. Previous versions of the genome sequence were highly fragmented, causing errors in the prediction of protein-coding genes and preventing the analysis of repetitive sequences and genome architecture. Here, we re-sequenced the genome using single-molecule real-time (SMRT) sequencing technology and, in combination with optical map data, this provided a gapless assembly of all twelve chromosomes except for the ribosomal DNA repeat cluster on chromosome 7. The more accurate gene annotation made possible by this new assembly revealed a large repertoire of secondary metabolism (SM) key genes (89) and putative biosynthetic pathways (77 SM gene clusters). The two mini-chromosomes differed from the ten core chromosomes in being repeat- and AT-rich and gene-poor but were significantly enriched with genes encoding putative secreted effector proteins. Transposable elements (TEs) were found to occupy 7% of the genome by length. Certain TE families showed a statistically significant association with effector genes and SM cluster genes and were transcriptionally active at particular stages of fungal development. All 24 subtelomeres were found to contain one of three highly- conserved repeat elements which, by providing sites for homologous recombination, were probably instrumental in four segmental duplications. The gapless genome of C. higginsianum provides access to repeat-rich regions that were previously poorly assembled, notably the mini-chromosomes and subtelomeres, and allowed prediction of the complete SM gene repertoire. It also provides insights into the potential role of TEs in gene and genome evolution and host adaptation in this asexual pathogen.
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spelling Dallery, Jean-FélixLapalu, NicolasZampounis, AntoniosPigné, SandrineLuyten, IsabelleAmselem, JoëlleWittenberg, Alexander H. J.Zhou, ShiguoQueiroz, Marisa V. deRobin, Guillaume P.Auger, AnnieHainaut, MatthieuHenrissat, BernardKim, Ki-TaeLee, Yong-HwanLespinet, OlivierSchwartz, David C.Thon, Michael R.Richard J. O’Connell2017-11-28T13:31:38Z2017-11-28T13:31:38Z2017-08-2914712164https://www.ncbi.nlm.nih.gov/pubmed/28851275http://www.locus.ufv.br/handle/123456789/13887The ascomycete fungus Colletotrichum higginsianum causes anthracnose disease of brassica crops and the model plant Arabidopsis thaliana. Previous versions of the genome sequence were highly fragmented, causing errors in the prediction of protein-coding genes and preventing the analysis of repetitive sequences and genome architecture. Here, we re-sequenced the genome using single-molecule real-time (SMRT) sequencing technology and, in combination with optical map data, this provided a gapless assembly of all twelve chromosomes except for the ribosomal DNA repeat cluster on chromosome 7. The more accurate gene annotation made possible by this new assembly revealed a large repertoire of secondary metabolism (SM) key genes (89) and putative biosynthetic pathways (77 SM gene clusters). The two mini-chromosomes differed from the ten core chromosomes in being repeat- and AT-rich and gene-poor but were significantly enriched with genes encoding putative secreted effector proteins. Transposable elements (TEs) were found to occupy 7% of the genome by length. Certain TE families showed a statistically significant association with effector genes and SM cluster genes and were transcriptionally active at particular stages of fungal development. All 24 subtelomeres were found to contain one of three highly- conserved repeat elements which, by providing sites for homologous recombination, were probably instrumental in four segmental duplications. The gapless genome of C. higginsianum provides access to repeat-rich regions that were previously poorly assembled, notably the mini-chromosomes and subtelomeres, and allowed prediction of the complete SM gene repertoire. It also provides insights into the potential role of TEs in gene and genome evolution and host adaptation in this asexual pathogen.engBMC Genomics18(1):667, Aug 2017Fungal genomeSMRT sequencingOptical mapTransposable elementsSecondary metabolism genesSubtelomeresSegmental duplicationAccessory chromosomesColletotrichum higginsianumGapless genome assembly of Colletotrichum higginsianum reveals chromosome structure and association of transposable elements with secondary metabolite gene clustersinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfinfo:eu-repo/semantics/openAccessreponame:LOCUS Repositório Institucional da UFVinstname:Universidade Federal de Viçosa (UFV)instacron:UFVORIGINALdocument.pdfdocument.pdfTexto completoapplication/pdf4384630https://locus.ufv.br//bitstream/123456789/13887/1/document.pdf95bf2fcc90526da243970c19b6298c1aMD51LICENSElicense.txtlicense.txttext/plain; charset=utf-81748https://locus.ufv.br//bitstream/123456789/13887/2/license.txt8a4605be74aa9ea9d79846c1fba20a33MD52THUMBNAILdocument.pdf.jpgdocument.pdf.jpgIM Thumbnailimage/jpeg5046https://locus.ufv.br//bitstream/123456789/13887/3/document.pdf.jpg042b02d30ce1f4b02565a25ce84afc0aMD53123456789/138872017-11-28 22:00:38.915oai:locus.ufv.br:123456789/13887Tk9URTogUExBQ0UgWU9VUiBPV04gTElDRU5TRSBIRVJFClRoaXMgc2FtcGxlIGxpY2Vuc2UgaXMgcHJvdmlkZWQgZm9yIGluZm9ybWF0aW9uYWwgcHVycG9zZXMgb25seS4KCk5PTi1FWENMVVNJVkUgRElTVFJJQlVUSU9OIExJQ0VOU0UKCkJ5IHNpZ25pbmcgYW5kIHN1Ym1pdHRpbmcgdGhpcyBsaWNlbnNlLCB5b3UgKHRoZSBhdXRob3Iocykgb3IgY29weXJpZ2h0Cm93bmVyKSBncmFudHMgdG8gRFNwYWNlIFVuaXZlcnNpdHkgKERTVSkgdGhlIG5vbi1leGNsdXNpdmUgcmlnaHQgdG8gcmVwcm9kdWNlLAp0cmFuc2xhdGUgKGFzIGRlZmluZWQgYmVsb3cpLCBhbmQvb3IgZGlzdHJpYnV0ZSB5b3VyIHN1Ym1pc3Npb24gKGluY2x1ZGluZwp0aGUgYWJzdHJhY3QpIHdvcmxkd2lkZSBpbiBwcmludCBhbmQgZWxlY3Ryb25pYyBmb3JtYXQgYW5kIGluIGFueSBtZWRpdW0sCmluY2x1ZGluZyBidXQgbm90IGxpbWl0ZWQgdG8gYXVkaW8gb3IgdmlkZW8uCgpZb3UgYWdyZWUgdGhhdCBEU1UgbWF5LCB3aXRob3V0IGNoYW5naW5nIHRoZSBjb250ZW50LCB0cmFuc2xhdGUgdGhlCnN1Ym1pc3Npb24gdG8gYW55IG1lZGl1bSBvciBmb3JtYXQgZm9yIHRoZSBwdXJwb3NlIG9mIHByZXNlcnZhdGlvbi4KCllvdSBhbHNvIGFncmVlIHRoYXQgRFNVIG1heSBrZWVwIG1vcmUgdGhhbiBvbmUgY29weSBvZiB0aGlzIHN1Ym1pc3Npb24gZm9yCnB1cnBvc2VzIG9mIHNlY3VyaXR5LCBiYWNrLXVwIGFuZCBwcmVzZXJ2YXRpb24uCgpZb3UgcmVwcmVzZW50IHRoYXQgdGhlIHN1Ym1pc3Npb24gaXMgeW91ciBvcmlnaW5hbCB3b3JrLCBhbmQgdGhhdCB5b3UgaGF2ZQp0aGUgcmlnaHQgdG8gZ3JhbnQgdGhlIHJpZ2h0cyBjb250YWluZWQgaW4gdGhpcyBsaWNlbnNlLiBZb3UgYWxzbyByZXByZXNlbnQKdGhhdCB5b3VyIHN1Ym1pc3Npb24gZG9lcyBub3QsIHRvIHRoZSBiZXN0IG9mIHlvdXIga25vd2xlZGdlLCBpbmZyaW5nZSB1cG9uCmFueW9uZSdzIGNvcHlyaWdodC4KCklmIHRoZSBzdWJtaXNzaW9uIGNvbnRhaW5zIG1hdGVyaWFsIGZvciB3aGljaCB5b3UgZG8gbm90IGhvbGQgY29weXJpZ2h0LAp5b3UgcmVwcmVzZW50IHRoYXQgeW91IGhhdmUgb2J0YWluZWQgdGhlIHVucmVzdHJpY3RlZCBwZXJtaXNzaW9uIG9mIHRoZQpjb3B5cmlnaHQgb3duZXIgdG8gZ3JhbnQgRFNVIHRoZSByaWdodHMgcmVxdWlyZWQgYnkgdGhpcyBsaWNlbnNlLCBhbmQgdGhhdApzdWNoIHRoaXJkLXBhcnR5IG93bmVkIG1hdGVyaWFsIGlzIGNsZWFybHkgaWRlbnRpZmllZCBhbmQgYWNrbm93bGVkZ2VkCndpdGhpbiB0aGUgdGV4dCBvciBjb250ZW50IG9mIHRoZSBzdWJtaXNzaW9uLgoKSUYgVEhFIFNVQk1JU1NJT04gSVMgQkFTRUQgVVBPTiBXT1JLIFRIQVQgSEFTIEJFRU4gU1BPTlNPUkVEIE9SIFNVUFBPUlRFRApCWSBBTiBBR0VOQ1kgT1IgT1JHQU5JWkFUSU9OIE9USEVSIFRIQU4gRFNVLCBZT1UgUkVQUkVTRU5UIFRIQVQgWU9VIEhBVkUKRlVMRklMTEVEIEFOWSBSSUdIVCBPRiBSRVZJRVcgT1IgT1RIRVIgT0JMSUdBVElPTlMgUkVRVUlSRUQgQlkgU1VDSApDT05UUkFDVCBPUiBBR1JFRU1FTlQuCgpEU1Ugd2lsbCBjbGVhcmx5IGlkZW50aWZ5IHlvdXIgbmFtZShzKSBhcyB0aGUgYXV0aG9yKHMpIG9yIG93bmVyKHMpIG9mIHRoZQpzdWJtaXNzaW9uLCBhbmQgd2lsbCBub3QgbWFrZSBhbnkgYWx0ZXJhdGlvbiwgb3RoZXIgdGhhbiBhcyBhbGxvd2VkIGJ5IHRoaXMKbGljZW5zZSwgdG8geW91ciBzdWJtaXNzaW9uLgo=Repositório InstitucionalPUBhttps://www.locus.ufv.br/oai/requestfabiojreis@ufv.bropendoar:21452017-11-29T01:00:38LOCUS Repositório Institucional da UFV - Universidade Federal de Viçosa (UFV)false
dc.title.en.fl_str_mv Gapless genome assembly of Colletotrichum higginsianum reveals chromosome structure and association of transposable elements with secondary metabolite gene clusters
title Gapless genome assembly of Colletotrichum higginsianum reveals chromosome structure and association of transposable elements with secondary metabolite gene clusters
spellingShingle Gapless genome assembly of Colletotrichum higginsianum reveals chromosome structure and association of transposable elements with secondary metabolite gene clusters
Dallery, Jean-Félix
Fungal genome
SMRT sequencing
Optical map
Transposable elements
Secondary metabolism genes
Subtelomeres
Segmental duplication
Accessory chromosomes
Colletotrichum higginsianum
title_short Gapless genome assembly of Colletotrichum higginsianum reveals chromosome structure and association of transposable elements with secondary metabolite gene clusters
title_full Gapless genome assembly of Colletotrichum higginsianum reveals chromosome structure and association of transposable elements with secondary metabolite gene clusters
title_fullStr Gapless genome assembly of Colletotrichum higginsianum reveals chromosome structure and association of transposable elements with secondary metabolite gene clusters
title_full_unstemmed Gapless genome assembly of Colletotrichum higginsianum reveals chromosome structure and association of transposable elements with secondary metabolite gene clusters
title_sort Gapless genome assembly of Colletotrichum higginsianum reveals chromosome structure and association of transposable elements with secondary metabolite gene clusters
author Dallery, Jean-Félix
author_facet Dallery, Jean-Félix
Lapalu, Nicolas
Zampounis, Antonios
Pigné, Sandrine
Luyten, Isabelle
Amselem, Joëlle
Wittenberg, Alexander H. J.
Zhou, Shiguo
Queiroz, Marisa V. de
Robin, Guillaume P.
Auger, Annie
Hainaut, Matthieu
Henrissat, Bernard
Kim, Ki-Tae
Lee, Yong-Hwan
Lespinet, Olivier
Schwartz, David C.
Thon, Michael R.
Richard J. O’Connell
author_role author
author2 Lapalu, Nicolas
Zampounis, Antonios
Pigné, Sandrine
Luyten, Isabelle
Amselem, Joëlle
Wittenberg, Alexander H. J.
Zhou, Shiguo
Queiroz, Marisa V. de
Robin, Guillaume P.
Auger, Annie
Hainaut, Matthieu
Henrissat, Bernard
Kim, Ki-Tae
Lee, Yong-Hwan
Lespinet, Olivier
Schwartz, David C.
Thon, Michael R.
Richard J. O’Connell
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Dallery, Jean-Félix
Lapalu, Nicolas
Zampounis, Antonios
Pigné, Sandrine
Luyten, Isabelle
Amselem, Joëlle
Wittenberg, Alexander H. J.
Zhou, Shiguo
Queiroz, Marisa V. de
Robin, Guillaume P.
Auger, Annie
Hainaut, Matthieu
Henrissat, Bernard
Kim, Ki-Tae
Lee, Yong-Hwan
Lespinet, Olivier
Schwartz, David C.
Thon, Michael R.
Richard J. O’Connell
dc.subject.pt-BR.fl_str_mv Fungal genome
SMRT sequencing
Optical map
Transposable elements
Secondary metabolism genes
Subtelomeres
Segmental duplication
Accessory chromosomes
Colletotrichum higginsianum
topic Fungal genome
SMRT sequencing
Optical map
Transposable elements
Secondary metabolism genes
Subtelomeres
Segmental duplication
Accessory chromosomes
Colletotrichum higginsianum
description The ascomycete fungus Colletotrichum higginsianum causes anthracnose disease of brassica crops and the model plant Arabidopsis thaliana. Previous versions of the genome sequence were highly fragmented, causing errors in the prediction of protein-coding genes and preventing the analysis of repetitive sequences and genome architecture. Here, we re-sequenced the genome using single-molecule real-time (SMRT) sequencing technology and, in combination with optical map data, this provided a gapless assembly of all twelve chromosomes except for the ribosomal DNA repeat cluster on chromosome 7. The more accurate gene annotation made possible by this new assembly revealed a large repertoire of secondary metabolism (SM) key genes (89) and putative biosynthetic pathways (77 SM gene clusters). The two mini-chromosomes differed from the ten core chromosomes in being repeat- and AT-rich and gene-poor but were significantly enriched with genes encoding putative secreted effector proteins. Transposable elements (TEs) were found to occupy 7% of the genome by length. Certain TE families showed a statistically significant association with effector genes and SM cluster genes and were transcriptionally active at particular stages of fungal development. All 24 subtelomeres were found to contain one of three highly- conserved repeat elements which, by providing sites for homologous recombination, were probably instrumental in four segmental duplications. The gapless genome of C. higginsianum provides access to repeat-rich regions that were previously poorly assembled, notably the mini-chromosomes and subtelomeres, and allowed prediction of the complete SM gene repertoire. It also provides insights into the potential role of TEs in gene and genome evolution and host adaptation in this asexual pathogen.
publishDate 2017
dc.date.accessioned.fl_str_mv 2017-11-28T13:31:38Z
dc.date.available.fl_str_mv 2017-11-28T13:31:38Z
dc.date.issued.fl_str_mv 2017-08-29
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dc.identifier.uri.fl_str_mv https://www.ncbi.nlm.nih.gov/pubmed/28851275
http://www.locus.ufv.br/handle/123456789/13887
dc.identifier.issn.none.fl_str_mv 14712164
identifier_str_mv 14712164
url https://www.ncbi.nlm.nih.gov/pubmed/28851275
http://www.locus.ufv.br/handle/123456789/13887
dc.language.iso.fl_str_mv eng
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dc.relation.ispartofseries.pt-BR.fl_str_mv 18(1):667, Aug 2017
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publisher.none.fl_str_mv BMC Genomics
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