Section: Genomics
Topic: Genetics/Genomics, Microbiology, Plant biology

Nucleosome patterns in four plant pathogenic fungi with contrasted genome structures

Clairet, Colin1 ; Lapalu, Nicolas1 ; Simon, Adeline1 ; Soyer, Jessica L.1, 2; Viaud, Muriel1; Zehraoui, Enric3 ; Dalmais, Berengère1; Fudal, Isabelle1  ; Ponts, Nadia3  
1 Université Paris-Saclay, INRAE, UR BIOGER, 91120 Palaiseau, France
2 Max Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, 24306 Plön, and Christian-Albrechts University of Kiel, Am Botanischen Garten 1-9, 24118 Kiel, Germany
3 INRAE, MycSA, F-33882 Villenave d’Ornon, 33140, France

Corresponding author(s): Fudal, Isabelle (isabelle.fudal@inrae.fr); Ponts, Nadia (nadia.ponts@inrae.fr)

10.24072/pcjournal.227 - Peer Community Journal, Volume 3 (2023), article no. e13.

Get full text PDF Peer reviewed and recommended by PCI
article image

Fungal pathogens represent a serious threat towards agriculture, health, and environment. Control of fungal diseases on crops necessitates a global understanding of fungal pathogenicity determinants and their expression during infection. Genomes of phytopathogenic fungi are often compartmentalized: the core genome contains housekeeping genes whereas the fast-evolving genome mainly contains transposable elements and species-specific genes. In this study, we analysed nucleosome landscapes of four phytopathogenic fungi with contrasted genome organizations to describe and compare nucleosome repartition patterns in relation with genome structure and gene expression level. We combined MNase-seq and RNA-seq analyses to concomitantly map nucleosome-rich and transcriptionally active regions during fungal growth in axenic culture; we developed the MNase-seq Tool Suite (MSTS) to analyse and visualise data obtained from MNase-seq experiments in combination with other genomic data and notably RNA-seq expression data. We observed different characteristics of nucleosome profiles between species, as well as between genomic regions within the same species. We further linked nucleosome repartition and gene expression. Our findings support that nucleosome positioning and occupancies are subjected to evolution, in relation with underlying genome sequence modifications. Understanding genomic organization and its role in expression regulation is the next gear to understand complex cellular mechanisms and their evolution.

Published online:
DOI: 10.24072/pcjournal.227
Type: Research article

Clairet, Colin 1; Lapalu, Nicolas 1; Simon, Adeline 1; Soyer, Jessica L. 1, 2; Viaud, Muriel 1; Zehraoui, Enric 3; Dalmais, Berengère 1; Fudal, Isabelle 1; Ponts, Nadia 3

1 Université Paris-Saclay, INRAE, UR BIOGER, 91120 Palaiseau, France
2 Max Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, 24306 Plön, and Christian-Albrechts University of Kiel, Am Botanischen Garten 1-9, 24118 Kiel, Germany
3 INRAE, MycSA, F-33882 Villenave d’Ornon, 33140, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_227,
     author = {Clairet, Colin and Lapalu, Nicolas and Simon, Adeline and Soyer, Jessica L. and Viaud, Muriel and Zehraoui, Enric and Dalmais, Bereng\`ere and Fudal, Isabelle and Ponts, Nadia},
     title = {Nucleosome patterns in four plant pathogenic fungi with contrasted genome structures},
     journal = {Peer Community Journal},
     eid = {e13},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.227},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.227/}
}
TY  - JOUR
AU  - Clairet, Colin
AU  - Lapalu, Nicolas
AU  - Simon, Adeline
AU  - Soyer, Jessica L.
AU  - Viaud, Muriel
AU  - Zehraoui, Enric
AU  - Dalmais, Berengère
AU  - Fudal, Isabelle
AU  - Ponts, Nadia
TI  - Nucleosome patterns in four plant pathogenic fungi with contrasted genome structures
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.227/
DO  - 10.24072/pcjournal.227
ID  - 10_24072_pcjournal_227
ER  - 
%0 Journal Article
%A Clairet, Colin
%A Lapalu, Nicolas
%A Simon, Adeline
%A Soyer, Jessica L.
%A Viaud, Muriel
%A Zehraoui, Enric
%A Dalmais, Berengère
%A Fudal, Isabelle
%A Ponts, Nadia
%T Nucleosome patterns in four plant pathogenic fungi with contrasted genome structures
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.227/
%R 10.24072/pcjournal.227
%F 10_24072_pcjournal_227
Clairet, Colin; Lapalu, Nicolas; Simon, Adeline; Soyer, Jessica L.; Viaud, Muriel; Zehraoui, Enric; Dalmais, Berengère; Fudal, Isabelle; Ponts, Nadia. Nucleosome patterns in four plant pathogenic fungi with contrasted genome structures. Peer Community Journal, Volume 3 (2023), article  no. e13. doi : 10.24072/pcjournal.227. https://peercommunityjournal.org/articles/10.24072/pcjournal.227/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.genomics.100014

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Amselem, J.; Cuomo, C. A.; van Kan, J. A. L.; Viaud, M.; Benito, E. P.; Couloux, A.; Coutinho, P. M.; de Vries, R. P.; Dyer, P. S.; Fillinger, S.; Fournier, E.; Gout, L.; Hahn, M.; Kohn, L.; Lapalu, N.; Plummer, K. M.; Pradier, J.-M.; Quévillon, E.; Sharon, A.; Simon, A.; ten Have, A.; Tudzynski, B.; Tudzynski, P.; Wincker, P.; Andrew, M.; Anthouard, V.; Beever, R. E.; Beffa, R.; Benoit, I.; Bouzid, O.; Brault, B.; Chen, Z.; Choquer, M.; Collémare, J.; Cotton, P.; Danchin, E. G.; Da Silva, C.; Gautier, A.; Giraud, C.; Giraud, T.; Gonzalez, C.; Grossetete, S.; Güldener, U.; Henrissat, B.; Howlett, B. J.; Kodira, C.; Kretschmer, M.; Lappartient, A.; Leroch, M.; Levis, C.; Mauceli, E.; Neuvéglise, C.; Oeser, B.; Pearson, M.; Poulain, J.; Poussereau, N.; Quesneville, H.; Rascle, C.; Schumacher, J.; Ségurens, B.; Sexton, A.; Silva, E.; Sirven, C.; Soanes, D. M.; Talbot, N. J.; Templeton, M.; Yandava, C.; Yarden, O.; Zeng, Q.; Rollins, J. A.; Lebrun, M.-H.; Dickman, M. Genomic Analysis of the Necrotrophic Fungal Pathogens Sclerotinia sclerotiorum and Botrytis cinerea, PLoS Genetics, Volume 7 (2011) no. 8 | DOI

[2] Balesdent, M. H.; Attard, A.; Ansan-Melayah, D.; Delourme, R.; Renard, M.; Rouxel, T. Genetic Control and Host Range of Avirulence Toward <i>Brassica napus</i> Cultivars Quinta and Jet Neuf in <i>Leptosphaeria maculans</i>, Phytopathology, Volume 91 (2001) no. 1, pp. 70-76 | DOI

[3] Barnes, T.; Korber, P. The Active Mechanism of Nucleosome Depletion by Poly(dA:dT) Tracts In Vivo, International Journal of Molecular Sciences, Volume 22 (2021) no. 15 | DOI

[4] Basenko, E.; Pulman, J.; Shanmugasundram, A.; Harb, O.; Crouch, K.; Starns, D.; Warrenfeltz, S.; Aurrecoechea, C.; Stoeckert, C.; Kissinger, J.; Roos, D.; Hertz-Fowler, C. FungiDB: An Integrated Bioinformatic Resource for Fungi and Oomycetes, Journal of Fungi, Volume 4 (2018) no. 1 | DOI

[5] Bolger, A. M.; Lohse, M.; Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, Volume 30 (2014) no. 15, pp. 2114-2120 | DOI

[6] Boutigny, A.-L.; Barreau, C.; Atanasova-Penichon, V.; Verdal-Bonnin, M.-N.; Pinson-Gadais, L.; Richard-Forget, F. Ferulic acid, an efficient inhibitor of type B trichothecene biosynthesis and Tri gene expression in Fusarium liquid cultures, Mycological Research, Volume 113 (2009) no. 6-7, pp. 746-753 | DOI

[7] Bunnik, E. M.; Polishko, A.; Prudhomme, J.; Ponts, N.; Gill, S. S.; Lonardi, S.; Le Roch, K. G. DNA-encoded nucleosome occupancy is associated with transcription levels in the human malaria parasite Plasmodium falciparum, BMC Genomics, Volume 15 (2014) no. 1 | DOI

[8] Chen, K.; Xi, Y.; Pan, X.; Li, Z.; Kaestner, K.; Tyler, J.; Dent, S.; He, X.; Li, W. DANPOS: Dynamic analysis of nucleosome position and occupancy by sequencing, Genome Research, Volume 23 (2012) no. 2, pp. 341-351 | DOI

[9] Cole, H. A.; Ocampo, J.; Iben, J. R.; Chereji, R. V.; Clark, D. J. Heavy transcription of yeast genes correlates with differential loss of histone H2B relative to H4 and queued RNA polymerases, Nucleic Acids Research, Volume 42 (2014) no. 20, pp. 12512-12522 | DOI

[10] Collemare, J.; O'Connell, R.; Lebrun, M. Nonproteinaceous effectors: the <i>terra incognita</i> of plant–fungal interactions, New Phytologist, Volume 223 (2019) no. 2, pp. 590-596 | DOI

[11] Collemare, J.; Seidl, M. F. Chromatin-dependent regulation of secondary metabolite biosynthesis in fungi: is the picture complete?, FEMS Microbiology Reviews, Volume 43 (2019) no. 6, pp. 591-607 | DOI

[12] Cook, D. E.; Kramer, H. M.; Torres, D. E.; Seidl, M. F.; Thomma, B. P. H. J. A unique chromatin profile defines adaptive genomic regions in a fungal plant pathogen, eLife, Volume 9 (2020) | DOI

[13] Core, L. J.; Waterfall, J. J.; Lis, J. T. Nascent RNA Sequencing Reveals Widespread Pausing and Divergent Initiation at Human Promoters, Science, Volume 322 (2008) no. 5909, pp. 1845-1848 | DOI

[14] Cuomo, C. A.; Güldener, U.; Xu, J.-R.; Trail, F.; Turgeon, B. G.; Di Pietro, A.; Walton, J. D.; Ma, L.-J.; Baker, S. E.; Rep, M.; Adam, G.; Antoniw, J.; Baldwin, T.; Calvo, S.; Chang, Y.-L.; DeCaprio, D.; Gale, L. R.; Gnerre, S.; Goswami, R. S.; Hammond-Kosack, K.; Harris, L. J.; Hilburn, K.; Kennell, J. C.; Kroken, S.; Magnuson, J. K.; Mannhaupt, G.; Mauceli, E.; Mewes, H.-W.; Mitterbauer, R.; Muehlbauer, G.; Münsterkötter, M.; Nelson, D.; O'Donnell, K.; Ouellet, T.; Qi, W.; Quesneville, H.; Roncero, M. I. G.; Seong, K.-Y.; Tetko, I. V.; Urban, M.; Waalwijk, C.; Ward, T. J.; Yao, J.; Birren, B. W.; Kistler, H. C. The <i>Fusarium graminearum</i> Genome Reveals a Link Between Localized Polymorphism and Pathogen Specialization, Science, Volume 317 (2007) no. 5843, pp. 1400-1402 | DOI

[15] Ding, Y.; Gardiner, D. M.; Kazan, K. Transcriptome analysis reveals infection strategies employed by Fusarium graminearum as a root pathogen, Microbiological Research, Volume 256 (2022) | DOI

[16] Dobin, A.; Davis, C. A.; Schlesinger, F.; Drenkow, J.; Zaleski, C.; Jha, S.; Batut, P.; Chaisson, M.; Gingeras, T. R. STAR: ultrafast universal RNA-seq aligner, Bioinformatics, Volume 29 (2012) no. 1, pp. 15-21 | DOI

[17] Diolez, A.; Marches, F.; Fortini, D.; Brygoo, Y. Boty, a long-terminal-repeat retroelement in the phytopathogenic fungus Botrytis cinerea, Applied and Environmental Microbiology, Volume 61 (1995) no. 1, pp. 103-108 | DOI

[18] Dutreux, F.; Da Silva, C.; d’Agata, L.; Couloux, A.; Gay, E. J.; Istace, B.; Lapalu, N.; Lemainque, A.; Linglin, J.; Noel, B.; Wincker, P.; Cruaud, C.; Rouxel, T.; Balesdent, M.-H.; Aury, J.-M. De novo assembly and annotation of three Leptosphaeria genomes using Oxford Nanopore MinION sequencing, Scientific Data, Volume 5 (2018) no. 1 | DOI

[19] Fisher, M. C.; Henk, D. A.; Briggs, C. J.; Brownstein, J. S.; Madoff, L. C.; McCraw, S. L.; Gurr, S. J. Emerging fungal threats to animal, plant and ecosystem health, Nature, Volume 484 (2012) no. 7393, pp. 186-194 | DOI

[20] Flores, O.; Orozco, M. nucleR: a package for non-parametric nucleosome positioning, Bioinformatics, Volume 27 (2011) no. 15, pp. 2149-2150 | DOI

[21] Fudal, I.; Ross, S.; Gout, L.; Blaise, F.; Kuhn, M. L.; Eckert, M. R.; Cattolico, L.; Bernard-Samain, S.; Balesdent, M. H.; Rouxel, T. Heterochromatin-Like Regions as Ecological Niches for Avirulence Genes in the <i>Leptosphaeria maculans</i> Genome: Map-Based Cloning of <i>AvrLm6</i>, Molecular Plant-Microbe Interactions, Volume 20 (2007) no. 4, pp. 459-470 | DOI

[22] Gay, E. J.; Soyer, J. L.; Lapalu, N.; Linglin, J.; Fudal, I.; Da Silva, C.; Wincker, P.; Aury, J.-M.; Cruaud, C.; Levrel, A.; Lemoine, J.; Delourme, R.; Rouxel, T.; Balesdent, M.-H. Large-scale transcriptomics to dissect 2 years of the life of a fungal phytopathogen interacting with its host plant, BMC Biology, Volume 19 (2021) no. 1 | DOI

[23] Ghassabi Kondalaji, S.; Bowman, G. D. Reb1, Cbf1, and Pho4 Bias Histone Sliding and Deposition Away from Their Binding Sites, Molecular and Cellular Biology, Volume 42 (2022) no. 2 | DOI

[24] Grandaubert, J.; Lowe, R. G.; Soyer, J. L.; Schoch, C. L.; Van de Wouw, A. P.; Fudal, I.; Robbertse, B.; Lapalu, N.; Links, M. G.; Ollivier, B.; Linglin, J.; Barbe, V.; Mangenot, S.; Cruaud, C.; Borhan, H.; Howlett, B. J.; Balesdent, M.-H.; Rouxel, T. Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens, BMC Genomics, Volume 15 (2014) no. 1 | DOI

[25] Hallen, H. E.; Huebner, M.; Shiu, S.-H.; Güldener, U.; Trail, F. Gene expression shifts during perithecium development in Gibberella zeae (anamorph Fusarium graminearum), with particular emphasis on ion transport proteins, Fungal Genetics and Biology, Volume 44 (2007) no. 11, pp. 1146-1156 | DOI

[26] Hawksworth, D. L.; Lücking, R. Fungal Diversity Revisited: 2.2 to 3.8 Million Species, Microbiology Spectrum, Volume 5 (2017) no. 4 | DOI

[27] Hornung, G.; Oren, M.; Barkai, N. Nucleosome Organization Affects the Sensitivity of Gene Expression to Promoter Mutations, Molecular Cell, Volume 46 (2012) no. 3, pp. 362-368 | DOI

[28] Hu, S.; Chen, X.; Liao, J.; Chen, Y.; Zhao, C.; Zhang, Y. CAM: A quality control pipeline for MNase-seq data, PLOS ONE, Volume 12 (2017) no. 8 | DOI

[29] Hughes, A. L.; Rando, O. J. Comparative Genomics Reveals Chd1 as a Determinant of Nucleosome Spacing <i>in Vivo</i>, G3 Genes|Genomes|Genetics, Volume 5 (2015) no. 9, pp. 1889-1897 | DOI

[30] Jiang, C.; Pugh, B. F. A compiled and systematic reference map of nucleosome positions across the Saccharomyces cerevisiae genome, Genome Biology, Volume 10 (2009) no. 10 | DOI

[31] Jin, H.; Finnegan, A. I.; Song, J. S. A unified computational framework for modeling genome-wide nucleosome landscape, Physical Biology, Volume 15 (2018) no. 6 | DOI

[32] Kaplan, N.; Moore, I. K.; Fondufe-Mittendorf, Y.; Gossett, A. J.; Tillo, D.; Field, Y.; LeProust, E. M.; Hughes, T. R.; Lieb, J. D.; Widom, J.; Segal, E. The DNA-encoded nucleosome organization of a eukaryotic genome, Nature, Volume 458 (2008) no. 7236, pp. 362-366 | DOI

[33] Kelloniemi, J.; Trouvelot, S.; Héloir, M.-C.; Simon, A.; Dalmais, B.; Frettinger, P.; Cimerman, A.; Fermaud, M.; Roudet, J.; Baulande, S.; Bruel, C.; Choquer, M.; Couvelard, L.; Duthieuw, M.; Ferrarini, A.; Flors, V.; Le Pêcheur, P.; Loisel, E.; Morgant, G.; Poussereau, N.; Pradier, J.-M.; Rascle, C.; Trdá, L.; Poinssot, B.; Viaud, M. Analysis of the Molecular Dialogue Between Gray Mold (<i>Botrytis cinerea</i>) and Grapevine (<i>Vitis vinifera</i>) Reveals a Clear Shift in Defense Mechanisms During Berry Ripening, Molecular Plant-Microbe Interactions, Volume 28 (2015) no. 11, pp. 1167-1180 | DOI

[34] King, R.; Urban, M.; Hammond-Kosack, M. C. U.; Hassani-Pak, K.; Hammond-Kosack, K. E. The completed genome sequence of the pathogenic ascomycete fungus Fusarium graminearum, BMC Genomics, Volume 16 (2015) no. 1 | DOI

[35] King, R.; Urban, M.; Hammond-Kosack, K. E. Annotation of Fusarium graminearum (PH-1) Version 5.0, Genome Announcements, Volume 5 (2017) no. 2 | DOI

[36] Krietenstein, N.; Wal, M.; Watanabe, S.; Park, B.; Peterson, C. L.; Pugh, B. F.; Korber, P. Genomic Nucleosome Organization Reconstituted with Pure Proteins, Cell, Volume 167 (2016) no. 3 | DOI

[37] Kwak, H.; Fuda, N. J.; Core, L. J.; Lis, J. T. Precise Maps of RNA Polymerase Reveal How Promoters Direct Initiation and Pausing, Science, Volume 339 (2013) no. 6122, pp. 950-953 | DOI

[38] Langmead, B.; Salzberg, S. L. Fast gapped-read alignment with Bowtie 2, Nature Methods, Volume 9 (2012) no. 4, pp. 357-359 | DOI

[39] Lantermann, A. B.; Straub, T.; Strålfors, A.; Yuan, G.-C.; Ekwall, K.; Korber, P. Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiae, Nature Structural & Molecular Biology, Volume 17 (2010) no. 2, pp. 251-257 | DOI

[40] Laurent, B.; Moinard, M.; Spataro, C.; Ponts, N.; Barreau, C.; Foulongne-Oriol, M. Landscape of genomic diversity and host adaptation in Fusarium graminearum, BMC Genomics, Volume 18 (2017) no. 1 | DOI

[41] Li, B.; Ruotti, V.; Stewart, R. M.; Thomson, J. A.; Dewey, C. N. RNA-Seq gene expression estimation with read mapping uncertainty, Bioinformatics, Volume 26 (2009) no. 4, pp. 493-500 | DOI

[42] Lieleg, C.; Ketterer, P.; Nuebler, J.; Ludwigsen, J.; Gerland, U.; Dietz, H.; Mueller-Planitz, F.; Korber, P. Nucleosome Spacing Generated by ISWI and CHD1 Remodelers Is Constant Regardless of Nucleosome Density, Molecular and Cellular Biology, Volume 35 (2015) no. 9, pp. 1588-1605 | DOI

[43] Lo Presti, L.; Lanver, D.; Schweizer, G.; Tanaka, S.; Liang, L.; Tollot, M.; Zuccaro, A.; Reissmann, S.; Kahmann, R. Fungal Effectors and Plant Susceptibility, Annual Review of Plant Biology, Volume 66 (2015) no. 1, pp. 513-545 | DOI

[44] Locke, G.; Haberman, D.; Johnson, S. M.; Morozov, A. V. Global remodeling of nucleosome positions in C. elegans, BMC Genomics, Volume 14 (2013) no. 1 | DOI

[45] Min, I. M.; Waterfall, J. J.; Core, L. J.; Munroe, R. J.; Schimenti, J.; Lis, J. T. Regulating RNA polymerase pausing and transcription elongation in embryonic stem cells, Genes & Development, Volume 25 (2011) no. 7, pp. 742-754 | DOI

[46] Nishida, H.; Motoyama, T.; Yamamoto, S.; Aburatani, H.; Osada, H. Genome-wide maps of mono- and di-nucleosomes of Aspergillus fumigatus, Bioinformatics, Volume 25 (2009) no. 18, pp. 2295-2297 | DOI

[47] Nishida, H.; Kondo, S.; Matsumoto, T.; Suzuki, Y.; Yoshikawa, H.; Taylor, T. D.; Sugiyama, J. Characteristics of nucleosomes and linker DNA regions on the genome of the basidiomycete <i>Mixia osmundae</i> revealed by mono- and dinucleosome mapping, Open Biology, Volume 2 (2012) no. 4 | DOI

[48] Oberbeckmann, E.; Krietenstein, N.; Niebauer, V.; Wang, Y.; Schall, K.; Moldt, M.; Straub, T.; Rohs, R.; Hopfner, K.-P.; Korber, P.; Eustermann, S. Genome information processing by the INO80 chromatin remodeler positions nucleosomes, Nature Communications, Volume 12 (2021) no. 1 | DOI

[49] Oberbeckmann, E.; Niebauer, V.; Watanabe, S.; Farnung, L.; Moldt, M.; Schmid, A.; Cramer, P.; Peterson, C. L.; Eustermann, S.; Hopfner, K.-P.; Korber, P. Ruler elements in chromatin remodelers set nucleosome array spacing and phasing, Nature Communications, Volume 12 (2021) no. 1 | DOI

[50] Ocampo, J.; Chereji, R. V.; Eriksson, P. R.; Clark, D. J. The ISW1 and CHD1 ATP-dependent chromatin remodelers compete to set nucleosome spacing <i>in vivo</i>, Nucleic Acids Research, Volume 44 (2016) no. 10, pp. 4625-4635 | DOI

[51] Ocampo, J.; Chereji, R. V.; Eriksson, P. R.; Clark, D. J. Contrasting roles of the RSC and ISW1/CHD1 chromatin remodelers in RNA polymerase II elongation and termination, Genome Research, Volume 29 (2019) no. 3, pp. 407-417 | DOI

[52] Pedro, H.; Yates, A. D.; Kersey, P. J.; De Silva, N. H. Collaborative Annotation Redefines Gene Sets for Crucial Phytopathogens, Frontiers in Microbiology, Volume 10 (2019) | DOI

[53] Ponts, N.; Harris, E. Y.; Prudhomme, J.; Wick, I.; Eckhardt-Ludka, C.; Hicks, G. R.; Hardiman, G.; Lonardi, S.; Le Roch, K. G. Nucleosome landscape and control of transcription in the human malaria parasite, Genome Research, Volume 20 (2010) no. 2, pp. 228-238 | DOI

[54] Porquier, A.; Morgant, G.; Moraga, J.; Dalmais, B.; Luyten, I.; Simon, A.; Pradier, J.-M.; Amselem, J.; Collado, I. G.; Viaud, M. The botrydial biosynthetic gene cluster of Botrytis cinerea displays a bipartite genomic structure and is positively regulated by the putative Zn(II)2Cys6 transcription factor BcBot6, Fungal Genetics and Biology, Volume 96 (2016), pp. 33-46 | DOI

[55] Porquier, A.; Tisserant, C.; Salinas, F.; Glassl, C.; Wange, L.; Enard, W.; Hauser, A.; Hahn, M.; Weiberg, A. Retrotransposons as pathogenicity factors of the plant pathogenic fungus Botrytis cinerea, Genome Biology, Volume 22 (2021) no. 1 | DOI

[56] Radman-Livaja, M.; Rando, O. J. Nucleosome positioning: How is it established, and why does it matter?, Developmental Biology, Volume 339 (2010) no. 2, pp. 258-266 | DOI

[57] Reyes, A. A.; Marcum, R. D.; He, Y. Structure and Function of Chromatin Remodelers, Journal of Molecular Biology, Volume 433 (2021) no. 14 | DOI

[58] Richmond, T. J.; Davey, C. A. The structure of DNA in the nucleosome core, Nature, Volume 423 (2003) no. 6936, pp. 145-150 | DOI

[59] Robinson, P. J. J.; Fairall, L.; Huynh, V. A. T.; Rhodes, D. EM measurements define the dimensions of the “30-nm” chromatin fiber: Evidence for a compact, interdigitated structure, Proceedings of the National Academy of Sciences, Volume 103 (2006) no. 17, pp. 6506-6511 | DOI

[60] Rouxel, T.; Grandaubert, J.; Hane, J. K.; Hoede, C.; van de Wouw, A. P.; Couloux, A.; Dominguez, V.; Anthouard, V.; Bally, P.; Bourras, S.; Cozijnsen, A. J.; Ciuffetti, L. M.; Degrave, A.; Dilmaghani, A.; Duret, L.; Fudal, I.; Goodwin, S. B.; Gout, L.; Glaser, N.; Linglin, J.; Kema, G. H. J.; Lapalu, N.; Lawrence, C. B.; May, K.; Meyer, M.; Ollivier, B.; Poulain, J.; Schoch, C. L.; Simon, A.; Spatafora, J. W.; Stachowiak, A.; Turgeon, B. G.; Tyler, B. M.; Vincent, D.; Weissenbach, J.; Amselem, J.; Quesneville, H.; Oliver, R. P.; Wincker, P.; Balesdent, M.-H.; Howlett, B. J. Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations, Nature Communications, Volume 2 (2011) no. 1 | DOI

[61] Russell, K.; Cheng, C.-H.; Bizzaro, J. W.; Ponts, N.; Emes, R. D.; Le Roch, K.; Marx, K. A.; Horrocks, P. Homopolymer tract organization in the human malarial parasite Plasmodium falciparum and related Apicomplexan parasites, BMC Genomics, Volume 15 (2014) no. 1 | DOI

[62] Sánchez-Vallet, A.; Fouché, S.; Fudal, I.; Hartmann, F. E.; Soyer, J. L.; Tellier, A.; Croll, D. The Genome Biology of Effector Gene Evolution in Filamentous Plant Pathogens, Annual Review of Phytopathology, Volume 56 (2018) no. 1, pp. 21-40 | DOI

[63] Satchwell, S. C.; Drew, H. R.; Travers, A. A. Sequence periodicities in chicken nucleosome core DNA, Journal of Molecular Biology, Volume 191 (1986) no. 4, pp. 659-675 | DOI

[64] Segal, E.; Fondufe-Mittendorf, Y.; Chen, L.; Thåström, A.; Field, Y.; Moore, I. K.; Wang, J.-P. Z.; Widom, J. A genomic code for nucleosome positioning, Nature, Volume 442 (2006) no. 7104, pp. 772-778 | DOI

[65] Segal, E.; Widom, J. Poly(dA:dT) tracts: major determinants of nucleosome organization, Current Opinion in Structural Biology, Volume 19 (2009) no. 1, pp. 65-71 | DOI

[66] Segal, E.; Widom, J. What controls nucleosome positions?, Trends in Genetics, Volume 25 (2009) no. 8, pp. 335-343 | DOI

[67] Shandilya, J.; Roberts, S. G. The transcription cycle in eukaryotes: From productive initiation to RNA polymerase II recycling, Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Volume 1819 (2012) no. 5, pp. 391-400 | DOI

[68] 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, Volume 31 (2015) no. 19, pp. 3210-3212 | DOI

[69] Simon, A.; Dalmais, B.; Morgant, G.; Viaud, M. Screening of a Botrytis cinerea one-hybrid library reveals a Cys2His2 transcription factor involved in the regulation of secondary metabolism gene clusters, Fungal Genetics and Biology, Volume 52 (2013), pp. 9-19 | DOI

[70] Singh, A. K.; Mueller-Planitz, F. Nucleosome Positioning and Spacing: From Mechanism to Function, Journal of Molecular Biology, Volume 433 (2021) no. 6 | DOI

[71] Soyer, J. L.; El Ghalid, M.; Glaser, N.; Ollivier, B.; Linglin, J.; Grandaubert, J.; Balesdent, M.-H.; Connolly, L. R.; Freitag, M.; Rouxel, T.; Fudal, I. Epigenetic Control of Effector Gene Expression in the Plant Pathogenic Fungus Leptosphaeria maculans, PLoS Genetics, Volume 10 (2014) no. 3 | DOI

[72] Soyer, J. L.; Möller, M.; Schotanus, K.; Connolly, L. R.; Galazka, J. M.; Freitag, M.; Stukenbrock, E. H. Chromatin analyses of Zymoseptoria tritici : Methods for chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-seq), Fungal Genetics and Biology, Volume 79 (2015), pp. 63-70 | DOI

[73] Soyer, J. L.; Balesdent, M.-H.; Rouxel, T.; Dean, R. A. To B or not to B: a tale of unorthodox chromosomes, Current Opinion in Microbiology, Volume 46 (2018), pp. 50-57 | DOI

[74] Soyer, J. L.; Clairet, C.; Gay, E. J.; Lapalu, N.; Rouxel, T.; Stukenbrock, E. H.; Fudal, I. Genome-wide mapping of histone modifications during axenic growth in two species of Leptosphaeria maculans showing contrasting genomic organization, Chromosome Research, Volume 29 (2021), pp. 219-236 | DOI

[75] Soyer, J. L.; Rouxel, T.; Fudal, I. Chromatin-based control of effector gene expression in plant-associated fungi, Current Opinion in Plant Biology, Volume 26 (2015), pp. 51-56 | DOI

[76] Struhl, K.; Segal, E. Determinants of nucleosome positioning, Nature Structural & Molecular Biology, Volume 20 (2013) no. 3, pp. 267-273 | DOI

[77] Szerlong, H. J.; Hansen, J. C. Nucleosome distribution and linker DNA: connecting nuclear function to dynamic chromatin structure, Biochemistry and Cell Biology, Volume 89 (2011) no. 1, pp. 24-34 | DOI

[78] Taylor, T. N.; Osborn, J. M. The importance of fungi in shaping the paleoecosystem, Review of Palaeobotany and Palynology, Volume 90 (1996) no. 3-4, pp. 249-262 | DOI

[79] Tillo, D.; Kaplan, N.; Moore, I. K.; Fondufe-Mittendorf, Y.; Gossett, A. J.; Field, Y.; Lieb, J. D.; Widom, J.; Segal, E.; Hughes, T. R. High Nucleosome Occupancy Is Encoded at Human Regulatory Sequences, PLoS ONE, Volume 5 (2010) no. 2 | DOI

[80] Tirosh, I.; Barkai, N. Two strategies for gene regulation by promoter nucleosomes, Genome Research, Volume 18 (2008) no. 7, pp. 1084-1091 | DOI

[81] Toruño, T. Y.; Stergiopoulos, I.; Coaker, G. Plant-Pathogen Effectors: Cellular Probes Interfering with Plant Defenses in Spatial and Temporal Manners, Annual Review of Phytopathology, Volume 54 (2016) no. 1, pp. 419-441 | DOI

[82] Tsankov, A. M.; Thompson, D. A.; Socha, A.; Regev, A.; Rando, O. J. The Role of Nucleosome Positioning in the Evolution of Gene Regulation, PLoS Biology, Volume 8 (2010) no. 7 | DOI

[83] Valouev, A.; Ichikawa, J.; Tonthat, T.; Stuart, J.; Ranade, S.; Peckham, H.; Zeng, K.; Malek, J. A.; Costa, G.; McKernan, K.; Sidow, A.; Fire, A.; Johnson, S. M. A high-resolution, nucleosome position map of <i>C. elegans</i> reveals a lack of universal sequence-dictated positioning, Genome Research, Volume 18 (2008) no. 7, pp. 1051-1063 | DOI

[84] Valouev, A.; Johnson, S. M.; Boyd, S. D.; Smith, C. L.; Fire, A. Z.; Sidow, A. Determinants of nucleosome organization in primary human cells, Nature, Volume 474 (2011) no. 7352, pp. 516-520 | DOI

[85] Van Kan, J. A. L.; Stassen, J. H. M.; Mosbach, A.; Van Der Lee, T. A. J.; Faino, L.; Farmer, A. D.; Papasotiriou, D. G.; Zhou, S.; Seidl, M. F.; Cottam, E.; Edel, D.; Hahn, M.; Schwartz, D. C.; Dietrich, R. A.; Widdison, S.; Scalliet, G. A gapless genome sequence of the fungus <i>Botrytis cinerea</i>, Molecular Plant Pathology, Volume 18 (2016) no. 1, pp. 75-89 | DOI

[86] Venters, B. J.; Pugh, B. F. A canonical promoter organization of the transcription machinery and its regulators in the <i>Saccharomyces</i> genome, Genome Research, Volume 19 (2009) no. 3, pp. 360-371 | DOI

[87] Wagner, F. R.; Dienemann, C.; Wang, H.; Stützer, A.; Tegunov, D.; Urlaub, H.; Cramer, P. Structure of SWI/SNF chromatin remodeller RSC bound to a nucleosome, Nature, Volume 579 (2020) no. 7799, pp. 448-451 | DOI

[88] Waterhouse, R. M.; Seppey, M.; Simão, F. A.; Manni, M.; Ioannidis, P.; Klioutchnikov, G.; Kriventseva, E. V.; Zdobnov, E. M. BUSCO Applications from Quality Assessments to Gene Prediction and Phylogenomics, Molecular Biology and Evolution, Volume 35 (2017) no. 3, pp. 543-548 | DOI

[89] Weiberg, A.; Wang, M.; Lin, F.-M.; Zhao, H.; Zhang, Z.; Kaloshian, I.; Huang, H.-D.; Jin, H. Fungal Small RNAs Suppress Plant Immunity by Hijacking Host RNA Interference Pathways, Science, Volume 342 (2013) no. 6154, pp. 118-123 | DOI

[90] Yague-Sanz, C.; Vázquez, E.; Sánchez, M.; Antequera, F.; Hermand, D. A conserved role of the RSC chromatin remodeler in the establishment of nucleosome-depleted regions, Current Genetics, Volume 63 (2016) no. 2, pp. 187-193 | DOI

[91] Yuan, G.-C.; Liu, Y.-J.; Dion, M. F.; Slack, M. D.; Wu, L. F.; Altschuler, S. J.; Rando, O. J. Genome-Scale Identification of Nucleosome Positions in <i>S. cerevisiae</i>, Science, Volume 309 (2005) no. 5734, pp. 626-630 | DOI

[92] Zhang, T.; Zhang, W.; Jiang, J. Genome-Wide Nucleosome Occupancy and Positioning and Their Impact on Gene Expression and Evolution in Plants, Plant Physiology, Volume 168 (2015) no. 4, pp. 1406-1416 | DOI

[93] Zhao, J.; Duan, W.; Xu, Y.; Zhang, C.; Wang, L.; Wang, J.; Tian, S.; Pei, G.; Zhan, G.; Zhuang, H.; Zhao, J.; Kang, Z. Distinct Transcriptomic Reprogramming in the Wheat Stripe Rust Fungus During the Initial Infection of Wheat and Barberry, Molecular Plant-Microbe Interactions, Volume 34 (2021) no. 2, pp. 198-209 | DOI

[94] Zhu, P.; Li, G. Structural insights of nucleosome and the 30-nm chromatin fiber, Current Opinion in Structural Biology, Volume 36 (2016), pp. 106-115 | DOI

Cited by Sources:

block.super