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

Botrytis cinerea strains infecting grapevine and tomato display contrasted repertoires of accessory chromosomes, transposons and small RNAs

Simon, Adeline1 ; Mercier, Alex1; Gladieux, Pierre2 ; Poinssot, Benoît3 ; Walker, Anne-Sophie1 ; Viaud, Muriel1  
1 Université Paris-Saclay, INRAE, UR BIOGER, 91120 Palaiseau, France
2 PHIM Plant Health Institute, Univ Montpellier, INRAE, CIRAD, Institut Agro, 34398 Montpellier, France
3 Agroécologie, CNRS, INRAE, Institut Agro Dijon, Univ. Bourgogne, Université Bourgogne Franche-Comté, 21000 Dijon, France

10.24072/pcjournal.211 - Peer Community Journal, Volume 2 (2022), article no. e83.

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The fungus Botrytis cinerea is a polyphagous pathogen that encompasses multiple host-specialized lineages. While several secreted proteins, secondary metabolites and retrotransposons-derived small RNAs have been characterized as virulence factors, their roles in host specialization remain unknown. The aim of this study was to identify the genomic correlates of host-specialization in populations of B. cinerea associated with grapevine and tomato. Using PacBio sequencing, we produced complete assemblies of the genomes of strains Sl3 and Vv3 that represent the French populations T and G1 of B. cinerea, specialized on tomato and grapevine, respectively. Both assemblies revealed 16 core chromosomes that were highly syntenic with chromosomes of the reference strain B05.10. The main sources of variation in gene content were the subtelomeric regions and the accessory chromosomes, especially the chromosome BCIN19 of Vv3 that was absent in Sl3 and B05.10. The repertoires and density of transposable elements were clearly different between the genomes of Sl3 and Vv3 with a larger number of subfamilies (26) and a greater genome coverage in Vv3 (7.7%) than in Sl3 (14 subfamilies, 4.5% coverage). An Helitron-like element was found in almost all subtelomeric regions of the Vv3 genome, in particular in the flanking regions of a highly duplicated gene encoding a Telomere-Linked Helicase, while both features were absent from the Sl3 and B05.10 genomes. Different retrotransposons in the Sl3 and the Vv3 strains resulted in the synthesis of distinct sets of small RNAs. Finally, extending the study to additional strains indicated that the accessory chromosome BCIN19 and the small RNAs producing retrotransposons Copia_4 and Gypsy_7 are common features of the G1 population that are scarcely if ever found in strains isolated from other populations. This research reveals that accessory chromosomes, repertoires of transposons and their derived small RNAs differ between populations of B. cinerea specialized on different hosts. The genomic data characterized in our study pave the way for further studies aiming at investigating the molecular mechanisms underpinning host specialization in a polyphagous pathogen.

Published online:
DOI: 10.24072/pcjournal.211
Type: Research article
Simon, Adeline 1; Mercier, Alex 1; Gladieux, Pierre 2; Poinssot, Benoît 3; Walker, Anne-Sophie 1; Viaud, Muriel 1

1 Université Paris-Saclay, INRAE, UR BIOGER, 91120 Palaiseau, France
2 PHIM Plant Health Institute, Univ Montpellier, INRAE, CIRAD, Institut Agro, 34398 Montpellier, France
3 Agroécologie, CNRS, INRAE, Institut Agro Dijon, Univ. Bourgogne, Université Bourgogne Franche-Comté, 21000 Dijon, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
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     title = {\protect\emph{Botrytis cinerea} strains infecting grapevine and tomato display contrasted repertoires of accessory chromosomes, transposons and small {RNAs}},
     journal = {Peer Community Journal},
     eid = {e83},
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Simon, Adeline; Mercier, Alex; Gladieux, Pierre; Poinssot, Benoît; Walker, Anne-Sophie; Viaud, Muriel. Botrytis cinerea strains infecting grapevine and tomato display contrasted repertoires of accessory chromosomes, transposons and small RNAs. Peer Community Journal, Volume 2 (2022), article  no. e83. doi : 10.24072/pcjournal.211. https://peercommunityjournal.org/articles/10.24072/pcjournal.211/

Peer reviewed and recommended by PCI : 10.24072/pci.genomics.100023

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] Amselem, J.; Lebrun, M.-H.; Quesneville, H. Whole genome comparative analysis of transposable elements provides new insight into mechanisms of their inactivation in fungal genomes, BMC Genomics, Volume 16 (2015) no. 1 | DOI

[3] Atwell, S.; Corwin, J. A.; Soltis, N. E.; Subedy, A.; Denby, K. J.; Kliebenstein, D. J. Whole genome resequencing of Botrytis cinerea isolates identifies high levels of standing diversity, Frontiers in Microbiology, Volume 6 (2015) | DOI

[4] Bertazzoni, S.; Williams, A. H.; Jones, D. A.; Syme, R. A.; Tan, K.-C.; Hane, J. K. Accessories Make the Outfit: Accessory Chromosomes and Other Dispensable DNA Regions in Plant-Pathogenic Fungi, Molecular Plant-Microbe Interactions®, Volume 31 (2018) no. 8, pp. 779-788 | DOI

[5] Blanco-Ulate, B.; Allen, G.; Powell, A. L. T.; Cantu, D. Draft Genome Sequence of Botrytis cinerea BcDW1, Inoculum for Noble Rot of Grape Berries, Genome Announcements, Volume 1 (2013) no. 3 | DOI

[6] Castanera, R.; Pérez, G.; López, L.; Sancho, R.; Santoyo, F.; Alfaro, M.; Gabaldón, T.; Pisabarro, A. G.; Oguiza, J. A.; Ramírez, L. Highly expressed captured genes and cross-kingdom domains present in Helitrons create novel diversity in Pleurotus ostreatus and other fungi, BMC Genomics, Volume 15 (2014) no. 1 | DOI

[7] Chellapan, B. V.; van Dam, P.; Rep, M.; Cornelissen, B. J. C.; Fokkens, L. Non-canonical Helitrons in Fusarium oxysporum, Mobile DNA, Volume 7 (2016) no. 1 | DOI

[8] Choquer, M.; Fournier, E.; Kunz, C.; Levis, C.; Pradier, J.-M.; Simon, A.; Viaud, M. Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen, FEMS Microbiology Letters, Volume 277 (2007) no. 1, pp. 1-10 | DOI

[9] Derbyshire, M.; Denton-Giles, M.; Hegedus, D.; Seifbarghy, S.; Rollins, J.; van Kan, J.; Seidl, M. F.; Faino, L.; Mbengue, M.; Navaud, O.; Raffaele, S.; Hammond-Kosack, K.; Heard, S.; Oliver, R. The Complete Genome Sequence of the Phytopathogenic Fungus Sclerotinia sclerotiorum Reveals Insights into the Genome Architecture of Broad Host Range Pathogens, Genome Biology and Evolution, Volume 9 (2017) no. 3, pp. 593-618 | DOI

[10] 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

[11] Drillon, G.; Carbone, A.; Fischer, G. SynChro: A Fast and Easy Tool to Reconstruct and Visualize Synteny Blocks along Eukaryotic Chromosomes, PLoS ONE, Volume 9 (2014) no. 3 | DOI

[12] Elad, Y.; Vivier, M.; Fillinger, S. Botrytis, the Good, the Bad and the Ugly, Botrytis – the Fungus, the Pathogen and its Management in Agricultural Systems, Springer International Publishing, Cham, 2015, pp. 1-15 | DOI

[13] Flutre, T.; Duprat, E.; Feuillet, C.; Quesneville, H. Considering Transposable Element Diversification in De Novo Annotation Approaches, PLoS ONE, Volume 6 (2011) no. 1 | DOI

[14] Fouché, S.; Oggenfuss, U.; Chanclud, E.; Croll, D. A devil's bargain with transposable elements in plant pathogens, Trends in Genetics, Volume 38 (2021) no. 3, pp. 222-230 | DOI

[15] Gao, W.; Khang, C. H.; Park, S.-Y.; Lee, Y.-H.; Kang, S. Evolution and Organization of a Highly Dynamic, Subtelomeric Helicase Gene Family in the Rice Blast Fungus Magnaporthe grisea, Genetics, Volume 162 (2002) no. 1, pp. 103-112 | DOI

[16] Geib, E.; Gressler, M.; Viediernikova, I.; Hillmann, F.; Jacobsen, I. D.; Nietzsche, S.; Hertweck, C.; Brock, M. A Non-canonical Melanin Biosynthesis Pathway Protects Aspergillus terreus Conidia from Environmental Stress, Cell Chemical Biology, Volume 23 (2016) no. 5, pp. 587-597 | DOI

[17] Gilchrist, C. L. M.; Chooi, Y.-H. clinker & clustermap.js: automatic generation of gene cluster comparison figures, Bioinformatics, Volume 37 (2021) no. 16, pp. 2473-2475 | DOI

[18] Gladieux, P.; Condon, B.; Ravel, S.; Soanes, D.; Maciel, J. L. N.; Nhani, A.; Chen, L.; Terauchi, R.; Lebrun, M.-H.; Tharreau, D.; Mitchell, T.; Pedley, K. F.; Valent, B.; Talbot, N. J.; Farman, M.; Fournier, E. Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus Magnaporthe oryzae, mBio, Volume 9 (2018) no. 1 | DOI

[19] Gurevich, A.; Saveliev, V.; Vyahhi, N.; Tesler, G. QUAST: quality assessment tool for genome assemblies, Bioinformatics, Volume 29 (2013) no. 8, pp. 1072-1075 | DOI

[20] Hoede, C.; Arnoux, S.; Moisset, M.; Chaumier, T.; Inizan, O.; Jamilloux, V.; Quesneville, H. PASTEC: An Automatic Transposable Element Classification Tool, PLoS ONE, Volume 9 (2014) no. 5 | DOI

[21] Kjærbølling, I.; Vesth, T.; Frisvad, J. C.; Nybo, J. L.; Theobald, S.; Kildgaard, S.; Petersen, T. I.; Kuo, A.; Sato, A.; Lyhne, E. K.; Kogle, M. E.; Wiebenga, A.; Kun, R. S.; Lubbers, R. J. M.; Mäkelä, M. R.; Barry, K.; Chovatia, M.; Clum, A.; Daum, C.; Haridas, S.; He, G.; LaButti, K.; Lipzen, A.; Mondo, S.; Pangilinan, J.; Riley, R.; Salamov, A.; Simmons, B. A.; Magnuson, J. K.; Henrissat, B.; Mortensen, U. H.; Larsen, T. O.; de Vries, R. P.; Grigoriev, I. V.; Machida, M.; Baker, S. E.; Andersen, M. R. A comparative genomics study of 23 Aspergillus species from section Flavi, Nature Communications, Volume 11 (2020) no. 1 | DOI

[22] Kojima, K. K. Structural and sequence diversity of eukaryotic transposable elements, Genes & Genetic Systems, Volume 94 (2019) no. 6, pp. 233-252 | DOI

[23] Koren, S.; Walenz, B. P.; Berlin, K.; Miller, J. R.; Bergman, N. H.; Phillippy, A. M. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation, Genome Research, Volume 27 (2017) no. 5, pp. 722-736 | DOI

[24] Levis, C.; Giraud, T.; Dutertre, M.; Fortini, D.; Brygoo, Y. Telomeric DNA of Botrytis cinerea: a useful tool for strain identification, FEMS Microbiology Letters, Volume 157 (1997) no. 2, pp. 267-272 | DOI

[25] Levis, C.; Fortini, D.; Brygoo, Y. Flipper, a mobile Fot1-like transposable element in Botrytis cinerea, Molecular and General Genetics MGG, Volume 254 (1997) no. 6, pp. 674-680 | DOI

[26] Lind, A. L.; Wisecaver, J. H.; Lameiras, C.; Wiemann, P.; Palmer, J. M.; Keller, N. P.; Rodrigues, F.; Goldman, G. H.; Rokas, A. Drivers of genetic diversity in secondary metabolic gene clusters within a fungal species, PLOS Biology, Volume 15 (2017) no. 11 | DOI

[27] Lombard, V.; Golaconda Ramulu, H.; Drula, E.; Coutinho, P. M.; Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013, Nucleic Acids Research, Volume 42 (2014) no. D1 | DOI

[28] Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet.journal, Volume 17 (2011) no. 1 | DOI

[29] Mbengue, M.; Navaud, O.; Peyraud, R.; Barascud, M.; Badet, T.; Vincent, R.; Barbacci, A.; Raffaele, S. Emerging Trends in Molecular Interactions between Plants and the Broad Host Range Fungal Pathogens Botrytis cinerea and Sclerotinia sclerotiorum, Frontiers in Plant Science, Volume 7 (2016) | DOI

[30] Meena, M.; Gupta, S. K.; Swapnil, P.; Zehra, A.; Dubey, M. K.; Upadhyay, R. S. Alternaria Toxins: Potential Virulence Factors and Genes Related to Pathogenesis, Frontiers in Microbiology, Volume 8 (2017) | DOI

[31] Mercier, A.; Carpentier, F.; Duplaix, C.; Auger, A.; Pradier, J.; Viaud, M.; Gladieux, P.; Walker, A. The polyphagous plant pathogenic fungus Botrytis cinerea encompasses host‐specialized and generalist populations, Environmental Microbiology, Volume 21 (2019) no. 12, pp. 4808-4821 | DOI

[32] Mercier, A.; Simon, A.; Lapalu, N.; Giraud, T.; Bardin, M.; Walker, A.-S.; Viaud, M.; Gladieux, P. Population Genomics Reveals Molecular Determinants of Specialization to Tomato in the Polyphagous Fungal Pathogen Botrytis cinerea in France, Phytopathology, Volume 111 (2021) no. 12, pp. 2355-2366 | DOI

[33] Olarte, R. A.; Menke, J.; Zhang, Y.; Sullivan, S.; Slot, J. C.; Huang, Y.; Badalamenti, J. P.; Quandt, A. C.; Spatafora, J. W.; Bushley, K. E. Chromosome rearrangements shape the diversification of secondary metabolism in the cyclosporin producing fungus Tolypocladium inflatum, BMC Genomics, Volume 20 (2019) no. 1 | DOI

[34] Plesken, C.; Pattar, P.; Reiss, B.; Noor, Z. N.; Zhang, L.; Klug, K.; Huettel, B.; Hahn, M. Genetic Diversity of Botrytis cinerea Revealed by Multilocus Sequencing, and Identification of B. cinerea Populations Showing Genetic Isolation and Distinct Host Adaptation, Frontiers in Plant Science, Volume 12 (2021) | DOI

[35] Porquier, A.; Moraga, J.; Morgant, G.; Dalmais, B.; Simon, A.; Sghyer, H.; Collado, I. G.; Viaud, M. Botcinic acid biosynthesis in Botrytis cinerea relies on a subtelomeric gene cluster surrounded by relics of transposons and is regulated by the Zn2Cys6 transcription factor BcBoa13, Current Genetics, Volume 65 (2019) no. 4, pp. 965-980 | DOI

[36] 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

[37] 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

[38] Quesneville, H.; Bergman, C. M.; Andrieu, O.; Autard, D.; Nouaud, D.; Ashburner, M.; Anxolabehere, D. Combined Evidence Annotation of Transposable Elements in Genome Sequences, PLoS Computational Biology, Volume 1 (2005) no. 2 | DOI

[39] Rehmeyer, C. J.; Li, W.; Kusaba, M.; Farman, M. L. The telomere-linked helicase (TLH) gene family in Magnaporthe oryzae: revised gene structure reveals a novel TLH-specific protein motif, Current Genetics, Volume 55 (2009) no. 3, pp. 253-262 | DOI

[40] Sánchez-Alonso, P.; Guzmán, P. Organization of Chromosome Ends in Ustilago maydis. RecQ-like Helicase Motifs at Telomeric Regions, Genetics, Volume 148 (1998) no. 3, pp. 1043-1054 | DOI

[41] Shumate, A.; Salzberg, S. L. Liftoff: accurate mapping of gene annotations, Bioinformatics, Volume 37 (2021) no. 12, pp. 1639-1643 | DOI

[42] 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

[43] Solovyev, V.; Kosarev, P.; Seledsov, I.; Vorobyev, D. Automatic annotation of eukaryotic genes, pseudogenes and promoters, Genome Biology, Volume 7 (2006) no. Suppl 1 | DOI

[44] Stukenbrock, E. H.; McDonald, B. A. The Origins of Plant Pathogens in Agro-Ecosystems, Annual Review of Phytopathology, Volume 46 (2008) no. 1, pp. 75-100 | DOI

[45] Tolios, A.; Teupser, D.; Holdt, L. M. Preanalytical Conditions and DNA Isolation Methods Affect Telomere Length Quantification in Whole Blood, PLOS ONE, Volume 10 (2015) no. 12 | DOI

[46] Valero-Jiménez, C. A.; Steentjes, M. B. F.; Slot, J. C.; Shi-Kunne, X.; Scholten, O. E.; van Kan, J. A. L. Dynamics in Secondary Metabolite Gene Clusters in Otherwise Highly Syntenic and Stable Genomes in the Fungal Genus Botrytis, Genome Biology and Evolution, Volume 12 (2020) no. 12, pp. 2491-2507 | DOI

[47] van Kan, J. A. L.; Goverse, A.; Vlugt-Bergmans, C. J. B. Electrophoretic karyotype analysis of Botrytis cinerea, Netherlands Journal of Plant Pathology, Volume 99 (1993) no. S3, pp. 119-128 | DOI

[48] 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 Botrytis cinerea, Molecular Plant Pathology, Volume 18 (2017) no. 1, pp. 75-89 | DOI

[49] Veloso, J.; van Kan, J. A. Many Shades of Grey in Botrytis–Host Plant Interactions, Trends in Plant Science, Volume 23 (2018) no. 7, pp. 613-622 | DOI

[50] Vigneault, F.; Ter-Ovanesyan, D.; Alon, S.; Eminaga, S.; C. Christodoulou, D.; Seidman, J. G.; Eisenberg, E.; M. Church, G. High-Throughput Multiplex Sequencing of miRNA, Current Protocols in Human Genetics, Volume 73, 2012, p. 11.12.1-11.12.10 | DOI

[51] Walker, A.-S. Diversity Within and Between Species of Botrytis, Botrytis – the Fungus, the Pathogen and its Management in Agricultural Systems, Springer International Publishing, Cham, 2015, pp. 91-125 | DOI

[52] Walker, A.-S.; Gladieux, P.; Decognet, V.; Fermaud, M.; Confais, J.; Roudet, J.; Bardin, M.; Bout, A.; C. Nicot, P.; Poncet, C.; Fournier, E. Population structure and temporal maintenance of the multihost fungal pathogen Botrytis cinerea: causes and implications for disease management, Environmental Microbiology, Volume 17 (2015) no. 4, pp. 1261-1274 | DOI

[53] Walker, B. J.; Abeel, T.; Shea, T.; Priest, M.; Abouelliel, A.; Sakthikumar, S.; Cuomo, C. A.; Zeng, Q.; Wortman, J.; Young, S. K.; Earl, A. M. Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement, PLoS ONE, Volume 9 (2014) no. 11 | DOI

[54] 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

[55] Wicker, T.; Sabot, F.; Hua-Van, A.; Bennetzen, J. L.; Capy, P.; Chalhoub, B.; Flavell, A.; Leroy, P.; Morgante, M.; Panaud, O.; Paux, E.; SanMiguel, P.; Schulman, A. H. A unified classification system for eukaryotic transposable elements, Nature Reviews Genetics, Volume 8 (2007) no. 12, pp. 973-982 | DOI

[56] Yang, H.; Yu, H.; Ma, L.-J. Accessory Chromosomes in Fusarium oxysporum, Phytopathology, Volume 110 (2020) no. 9, pp. 1488-1496 | DOI

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