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1. Nucleosome patterns in four plant pathogenic fungi with contrasted genome structures

Author

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

Subjects
Archaeology, CC1-960, Science
Abstract

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
2023
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10. The neighbouring genes AvrLm10A and AvrLm10B are part of a large multigene family of cooperating effector genes conserved in Dothideomycetes and Sordariomycetes

Author

Talbi, Nacera, primary, Fokkens, Like, additional, Audran, Corinne, additional, Petit‐Houdenot, Yohann, additional, Pouzet, Cécile, additional, Blaise, Françoise, additional, Gay, Elise J., additional, Rouxel, Thierry, additional, Balesdent, Marie‐Hélène, additional, Rep, Martijn, additional, and Fudal, Isabelle, additional

Published
2023
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11. The neighbouring genes AvrLm10A and AvrLm10B are part of a large multigene family of cooperating effector genes conserved in Dothideomycetes and Sordariomycetes

Author

Talbi, Nacera, Fokkens, Like, Audran, Corinne, Petit‐Houdenot, Yohann, Pouzet, Cécile, Blaise, Françoise, Gay, Elise J., Rouxel, Thierry, Balesdent, Marie Hélène, Rep, Martijn, Fudal, Isabelle, Talbi, Nacera, Fokkens, Like, Audran, Corinne, Petit‐Houdenot, Yohann, Pouzet, Cécile, Blaise, Françoise, Gay, Elise J., Rouxel, Thierry, Balesdent, Marie Hélène, Rep, Martijn, and Fudal, Isabelle

Abstract

Fungal effectors (small-secreted proteins) have long been considered as species or even subpopulation-specific. The increasing availability of high-quality fungal genomes and annotations has allowed the identification of trans-species or trans-genera families of effectors. Two avirulence effectors, AvrLm10A and AvrLm10B, of Leptosphaeria maculans, the fungus causing stem canker of oilseed rape, are members of such a large family of effectors. AvrLm10A and AvrLm10B are neighbouring genes, organized in divergent transcriptional orientation. Sequence searches within the L. maculans genome showed that AvrLm10A/AvrLm10B belong to a multigene family comprising five pairs of genes with a similar tail-to-tail organization. The two genes, in a pair, always had the same expression pattern and two expression profiles were distinguished, associated with the biotrophic colonization of cotyledons and/or petioles and stems. Of the two protein pairs further investigated, AvrLm10A_like1/AvrLm10B_like1 and AvrLm10A_like2/AvrLm10B_like2, the second one had the ability to physically interact, similarly to what was previously described for the AvrLm10A/AvrLm10B pair, and cross-interactions were also detected for two pairs. AvrLm10A homologues were identified in more than 30 Dothideomycete and Sordariomycete plant-pathogenic fungi. One of them, SIX5, is an effector from Fusarium oxysporum f. sp. lycopersici physically interacting with the avirulence effector Avr2. We found that AvrLm10A/SIX5 homologues were associated with at least eight distinct putative effector families, suggesting that AvrLm10A/SIX5 is able to cooperate with different effectors. These results point to a general role of the AvrLm10A/SIX5 proteins as “cooperating proteins”, able to interact with diverse families of effectors whose encoding gene is co-regulated with the neighbouring AvrLm10A homologue.

Published
2023

13. Improving sustainable crop protection using population genetics concepts

Author

Saubin, Méline, primary, Louet, Clémentine, additional, Bousset, Lydia, additional, Fabre, Frédéric, additional, Frey, Pascal, additional, Fudal, Isabelle, additional, Grognard, Frédéric, additional, Hamelin, Frédéric, additional, Mailleret, Ludovic, additional, Stoeckel, Solenn, additional, Touzeau, Suzanne, additional, Petre, Benjamin, additional, and Halkett, Fabien, additional

Published
2022
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14. A new family of structurally conserved fungal effectors displays epistatic interactions with plant resistance proteins

Author

Lazar, Noureddine, primary, Mesarich, Carl H., additional, Petit-Houdenot, Yohann, additional, Talbi, Nacera, additional, Li de la Sierra-Gallay, Ines, additional, Zélie, Emilie, additional, Blondeau, Karine, additional, Gracy, Jérôme, additional, Ollivier, Bénédicte, additional, Blaise, Françoise, additional, Rouxel, Thierry, additional, Balesdent, Marie-Hélène, additional, Idnurm, Alexander, additional, van Tilbeurgh, Herman, additional, and Fudal, Isabelle, additional

Published
2022
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15. Local Rather than Global H3K27me3 Dynamics Are Associated with Differential Gene Expression in Verticillium dahliae

Author

Kramer, Martin, Seidl, Michael F., Thomma, Bart P.H.J., Cook, David E., Fudal, Isabelle, Di Pietro, Antonio, Kramer, Martin, Seidl, Michael F., Thomma, Bart P.H.J., Cook, David E., Fudal, Isabelle, and Di Pietro, Antonio

Abstract

Differential growth conditions typically trigger global transcriptional responses in filamentous fungi. Such fungal responses to environmental cues involve epigenetic regulation, including chemical histone modifications. It has been proposed that conditionally expressed genes, such as those that encode secondary metabolites but also effectors in pathogenic species, are often associated with a specific histone modification, lysine27 methylation of H3 (H3K27me3). However, thus far, no analyses on the global H3K27me3 profiles have been reported under differential growth conditions in order to assess if H3K27me3 dynamics govern differential transcription. Using chromatin immunoprecipitation sequencing (ChIP-seq) and RNA sequencing data from the plant-pathogenic fungus Verticillium dahliae grown in three in vitro cultivation media, we now show that a substantial number of the identified H3K27me3 domains globally display stable profiles among these growth conditions. However, we observe local quantitative differences in H3K27me3 ChIP-seq signals that are associated with a subset of differentially transcribed genes between media. Comparing the in vitro results to expression during plant infection suggests that in planta-induced genes may require chromatin remodeling to achieve expression. Overall, our results demonstrate that some loci display H3K27me3 dynamics associated with concomitant transcriptional variation, but many differentially expressed genes are associated with stable H3K27me3 domains. Thus, we conclude that while H3K27me3 is required for transcriptional repression, it does not appear that transcriptional activation requires the global erasure of H3K27me3. We propose that the H3K27me3 domains that do not undergo dynamic methylation may contribute to transcription through other mechanisms or may serve additional genomic regulatory functions.

Published
2022

16. Improving sustainable crop protection using population genetics concepts.

Author

Saubin, Méline, Louet, Clémentine, Bousset, Lydia, Fabre, Frédéric, Frey, Pascal, Fudal, Isabelle, Grognard, Frédéric, Hamelin, Frédéric, Mailleret, Ludovic, Stoeckel, Solenn, Touzeau, Suzanne, Petre, Benjamin, and Halkett, Fabien

Subjects
POPULATION genetics, PLANT breeding, PLANT-pathogen relationships, POPULATION dynamics, PHYTOPATHOGENIC microorganisms
Abstract

Growing genetically resistant plants allows pathogen populations to be controlled and reduces the use of pesticides. However, pathogens can quickly overcome such resistance. In this context, how can we achieve sustainable crop protection? This crucial question has remained largely unanswered despite decades of intense debate and research effort. In this study, we used a bibliographic analysis to show that the research field of resistance durability has evolved into three subfields: (1) "plant breeding" (generating new genetic material), (2) "molecular interactions" (exploring the molecular dialogue governing plant–pathogen interactions) and (3) "epidemiology and evolution" (explaining and forecasting of pathogen population dynamics resulting from selection pressure[s] exerted by resistant plants). We argue that this triple split of the field impedes integrated research progress and ultimately compromises the sustainable management of genetic resistance. After identifying a gap among the three subfields, we argue that the theoretical framework of population genetics could bridge this gap. Indeed, population genetics formally explains the evolution of all heritable traits, and allows genetic changes to be tracked along with variation in population dynamics. This provides an integrated view of pathogen adaptation, in particular via evolutionary–epidemiological feedbacks. In this Opinion Note, we detail examples illustrating how such a framework can better inform best practices for developing and managing genetically resistant cultivars. [ABSTRACT FROM AUTHOR]

Published
2023
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17. The neighboring genes AvrLm10A and AvrLm10B are part of a large multigene family of cooperating effector genes conserved in Dothideomycetes and Sordariomycetes

Author

Talbi, Nacera, primary, Fokkens, Like, additional, Audran, Corinne, additional, Petit-Houdenot, Yohann, additional, Pouzet, Cécile, additional, Blaise, Françoise, additional, Gay, Elise, additional, Rouxel, Thierry, additional, Balesdent, Marie-Hélène, additional, Rep, Martijn, additional, and Fudal, Isabelle, additional

Published
2022
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19. Improving the design of sustainable crop protection strategies thanks to population genetics concepts

Author

Saubin, Méline, Louet, Clémentine, Bousset, Lydia, Fabre, Frédéric, Fudal, Isabelle, Grognard, Frédéric, Mailleret, Ludovic, Stoeckel, Solenn, Touzeau, Suzanne, Petre, Benjamin, Halkett, Fabien, Interactions Arbres-Microorganismes (IAM), Université de Lorraine (UL)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Santé et agroécologie du vignoble (UMR SAVE), Université de Bordeaux (UB)-Institut des Sciences de la Vigne et du Vin (ISVV)-Ecole Nationale Supérieure des Sciences Agronomiques de Bordeaux-Aquitaine (Bordeaux Sciences Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), BIOlogie et GEstion des Risques en agriculture (BIOGER), AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Biological control of artificial ecosystems (BIOCORE), Inria Sophia Antipolis - Méditerranée (CRISAM), Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-Laboratoire d'océanographie de Villefranche (LOV), Institut national des sciences de l'Univers (INSU - CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut de la Mer de Villefranche (IMEV), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut de la Mer de Villefranche (IMEV), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut Sophia Agrobiotech (ISA), Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-INSTITUT AGRO Agrocampus Ouest, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Université Nice Sophia Antipolis (1965 - 2019) (UNS), and COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Côte d'Azur (UCA)

Subjects
[SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE], [MATH.MATH-GM]Mathematics [math]/General Mathematics [math.GM], food and beverages, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

Cropping genetically resistant plants allows to control pathogen populations while substantially reducing chemical inputs. However, resistances are often quickly defeated by pathogens. In this context, how can sustainable crop protection be achieved? This question has shaped the debate about the durability of genetic resistances in agriculture for decades, and, despite active research efforts, has not been satisfactorily answered yet. Here we demonstrate from a bibliography analysis that the research field of resistance durability evolved into two non-overlapping directions: (i) the subfield of 'epidemiology and evolution', which aims to forecast and explain pathogen population dynamics; (ii) the subfield of 'molecular interactions', which studies the molecular processes involved in the overcoming of resistance and in the dialogue between plants and pathogens. After reviewing briefly these two subfields and the gap between the corresponding research communities, we propose strategies to merge these approaches into one by using the concepts of population genetics. Ultimately, such new eco-evolutionary studies could be used to determine the best strategy for the deployment of genetically resistant cultivars by integrating, from gene to landscape, all relevant and contextual biological knowledge into sound theoretical models.

Published
2021

20. A new avirulence gene of Leptosphaeria maculans , AvrLm14 , identifies a resistance source in American broccoli ( Brassica oleracea ) genotypes

Author

Degrave, Alexandre, Wagner, Marine, George, Pierre, Coudard, Laurent, Pinochet, Xavier, Ermel, Magali, Gay, Elise, Fudal, Isabelle, Moreno‐Rico, Onesimo, Rouxel, Thierry, Balesdent, Marie‐Hélène, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), BIOlogie et GEstion des Risques en agriculture (BIOGER), AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), innolea, Terres Inovia, Universidad Autónoma de Aguascalientes, ANR-17-EURE-0007,SPS-GSR,Ecole Universitaire de Recherche de Sciences des Plantes de Paris-Saclay(2017), Université de Rennes (UR)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-INSTITUT AGRO Agrocampus Ouest, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), and ANR GPLA07‐024C, Agence Nationale de la Recherche

Subjects
Genotype, [SDV]Life Sciences [q-bio], Brassica napus, food and beverages, gene‐for‐gene, Original Articles, Brassica, stem canker, resistance introgression, Ascomycota, [SDE]Environmental Sciences, gene-for-gene, Original Article, Leptosphaeria, Plant Diseases
Abstract

In many cultivated crops, sources of resistance to diseases are sparse and rely on introgression from wild relatives. Agricultural crops often are allopolyploids resulting from interspecific crosses between related species, which are sources of diversity for resistance genes. This is the case for Brassica napus (oilseed rape, canola), an interspecific hybrid between Brassica rapa (turnip) and Brassica oleracea (cabbage). B. napus has a narrow genetic basis and few effective resistance genes against stem canker (blackleg) disease, caused by the fungus Leptosphaeria maculans, are currently available. B. rapa diversity has proven to be a valuable source of resistance (Rlm, LepR) genes, while B. oleracea genotypes were mostly considered susceptible. Here we identified a new resistance source in B. oleracea genotypes from America, potentially effective against French L. maculans isolates under both controlled and field conditions. Genetic analysis of fungal avirulence and subsequent cloning and validation identified a new avirulence gene termed AvrLm14 and suggested a typical gene‐for‐gene interaction between AvrLm14 and the postulated Rlm14 gene. AvrLm14 shares all the usual characteristics of L. maculans avirulence genes: it is hosted in a genomic region enriched in transposable elements and heterochromatin marks H3K9me3, its expression is repressed during vegetative growth but shows a strong overexpression 5–9 days following cotyledon infection, and it encodes a small secreted protein enriched in cysteine residues with few matches in databases. Similar to the previously cloned AvrLm10‐A, AvrLm14 contributes to reduce lesion size on susceptible cotyledons, pointing to a complex interplay between effectors promoting or reducing lesion development., Cloning of avirulence gene AvrLm14 in Leptosphaeria maculans allowed us to identify the first resistance gene to the fungus in Brassica oleracea; therefore B. oleracea diversity may be exploited to find novel resistance to the disease.

Published
2021

22. Crystal structure of the effector AvrLm4–7 of Leptosphaeria maculans reveals insights into its translocation into plant cells and recognition by resistance proteins

Author

Blondeau, Karine, Blaise, Françoise, Graille, Marc, Kale, Shiv D., Linglin, Juliette, Ollivier, Bénédicte, Labarde, Audrey, Lazar, Noureddine, Daverdin, Guillaume, Balesdent, Marie-Hélène, Choi, Danielle H.Y., Tyler, Brett M., Rouxel, Thierry, van Tilbeurgh, Herman, and Fudal, Isabelle

Published
2015
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23. A gene‐for‐gene interaction involving a ‘late’ effector contributes to quantitative resistance to the stem canker disease in Brassica napus

Author

JIQUEL, Audren, Gervais, Julie, Geistodt‐Kiener, Aude, Delourme, Régine, GAY, Elise, Ollivier, Bénédicte, Fudal, Isabelle, Faure, Sébastien, Balesdent, Marie‐Hélène, Rouxel, Thierry, BIOlogie et GEstion des Risques en agriculture (BIOGER), AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Euralis Semences, Université Paris Saclay, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), innolea, 2017/1374, Association Nationale de la Recherche et de la Technologie, SOFIPROTEOL, Terres Inovia, INRAE SPE, ANR-17-EURE-0007,SPS-GSR,Ecole Universitaire de Recherche de Sciences des Plantes de Paris-Saclay(2017), Université de Rennes (UR)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-INSTITUT AGRO Agrocampus Ouest, and Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)

Subjects
Leptosphaeria maculans, effector, quantitative disease resistance, [SDV]Life Sciences [q-bio], Brassica napus, [SDE]Environmental Sciences, gene-for-gene interaction
Abstract

Early Access; International audience; The control of stem canker disease of Brassica napus (rapeseed), caused by the fungus Leptosphaeria maculans is largely based on plant genetic resistance: single-gene specific resistance (Rlm genes) or quantitative, polygenic, adult-stage resistance. Our working hypothesis was that quantitative resistance partly obeys the gene-for-gene model, with resistance genes "recognizing" fungal effectors expressed during late systemic colonization. Five LmSTEE (stem-expressed effector) genes were selected and placed under the control of the AvrLm4-7 promoter, an effector gene highly expressed at the cotyledon stage of infection, for miniaturized cotyledon inoculation test screening of a gene pool of 204 rapeseed genotypes. We identified a rapeseed genotype, 'Yudal', expressing hypersensitive response to LmSTEE98. The LmSTEE98-RlmSTEE98 interaction was further validated by inactivation of the LmSTEE98 gene with a CRISPR-Cas9 approach. Isolates with mutated versions of LmSTEE98 induced more severe stem symptoms than the wild-type isolate in 'Yudal'. This single-gene resistance was mapped in a 0.6 cM interval of the 'Darmor_bzh' x 'Yudal' genetic map. One typical gene-for-gene interaction contributes partly to quantitative resistance when L. maculans colonizes the stems of rapeseed. With numerous other effectors specific to stem colonization, our study provides a new route for resistance gene discovery, elucidation of quantitative resistance mechanisms, and selection for durable resistance.This article is protected by copyright. All rights reserved.

Published
2021

24. Additional file 6 of Large-scale transcriptomics to dissect 2 years of the life of a fungal phytopathogen interacting with its host plant

Author

Gay, Elise J., Soyer, Jessica L., Lapalu, Nicolas, Linglin, Juliette, Fudal, Isabelle, Silva, Corinne Da, Wincker, Patrick, Jean-Marc Aury, Cruaud, Corinne, Levrel, Anne, Lemoine, Jocelyne, Delourme, Regine, Rouxel, Thierry, and Balesdent, Marie-Hélène

Abstract

Additional file 6: S3 Text. Generation of a new repertoire of small secreted proteins considered as candidate effectors.

Published
2021
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25. Additional file 2 of Large-scale transcriptomics to dissect 2 years of the life of a fungal phytopathogen interacting with its host plant

Author

Gay, Elise J., Soyer, Jessica L., Lapalu, Nicolas, Linglin, Juliette, Fudal, Isabelle, Silva, Corinne Da, Wincker, Patrick, Jean-Marc Aury, Cruaud, Corinne, Levrel, Anne, Lemoine, Jocelyne, Delourme, Regine, Rouxel, Thierry, and Balesdent, Marie-Hélène

Abstract

Additional file 2: Table S1. Results of the mapping parameters tested for distinguishing between reads from L. maculans and L. biglobosa. (PDF 37 kb)

Published
2021
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26. Additional file 16 of Large-scale transcriptomics to dissect 2 years of the life of a fungal phytopathogen interacting with its host plant

Author

Gay, Elise J., Soyer, Jessica L., Lapalu, Nicolas, Linglin, Juliette, Fudal, Isabelle, Silva, Corinne Da, Wincker, Patrick, Jean-Marc Aury, Cruaud, Corinne, Levrel, Anne, Lemoine, Jocelyne, Delourme, Regine, Rouxel, Thierry, and Balesdent, Marie-Hélène

Abstract

Additional file 16: S4 Text. Comparison between the v1 and v2 versions of gene model annotations.

Published
2021
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27. Additional file 4 of Large-scale transcriptomics to dissect 2 years of the life of a fungal phytopathogen interacting with its host plant

Author

Gay, Elise J., Soyer, Jessica L., Lapalu, Nicolas, Linglin, Juliette, Fudal, Isabelle, Silva, Corinne Da, Wincker, Patrick, Jean-Marc Aury, Cruaud, Corinne, Levrel, Anne, Lemoine, Jocelyne, Delourme, Regine, Rouxel, Thierry, and Balesdent, Marie-Hélène

Abstract

Additional file 4: S2 Text. Reproducibility between replicates.

Published
2021
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28. Large-scale transcriptomics to dissect 2 years of the life of a fungal phytopathogen interacting with its host plant

Author

Gay, Elise, Soyer, Jessica, Lapalu, Nicolas, LINGLIN, Juliette, Fudal, Isabelle, Da Silva, Corinne, Wincker, Patrick, Aury, Jean-Marc, Cruaud, Corinne, Levrel, Anne, Lemoine, Jocelyne, Delourme, Régine, Rouxel, Thierry, Balesdent, Marie-Hélène, BIOlogie et GEstion des Risques en agriculture (BIOGER), AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Institut de Biologie François JACOB (JACOB), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Université de Rennes (UR)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-INSTITUT AGRO Agrocampus Ouest, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Promosol (METAPHOR project), France Genomique (Leptolife project), ANR-17-EURE-0007,SPS-GSR,Ecole Universitaire de Recherche de Sciences des Plantes de Paris-Saclay(2017), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, and Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)

Subjects
Leptosphaeria maculans, Chromatin regulation, Brassica napus, Genes, Fungal, Pathogenesis, Lifestyle transitions, Effectors, Fungal Proteins, Fungal biology, Expression waves, lcsh:Biology (General), [SDE]Environmental Sciences, Host-Pathogen Interactions, Transcriptome, Transcriptomics, lcsh:QH301-705.5, Leptosphaeria, Plant Diseases, Research Article
Abstract

Background The fungus Leptosphaeria maculans has an exceptionally long and complex relationship with its host plant, Brassica napus, during which it switches between different lifestyles, including asymptomatic, biotrophic, necrotrophic, and saprotrophic stages. The fungus is also exemplary of “two-speed” genome organisms in the genome of which gene-rich and repeat-rich regions alternate. Except for a few stages of plant infection under controlled conditions, nothing is known about the genes mobilized by the fungus throughout its life cycle, which may last several years in the field. Results We performed RNA-seq on samples corresponding to all stages of the interaction of L. maculans with its host plant, either alive or dead (stem residues after harvest) in controlled conditions or in field experiments under natural inoculum pressure, over periods of time ranging from a few days to months or years. A total of 102 biological samples corresponding to 37 sets of conditions were analyzed. We show here that about 9% of the genes of this fungus are highly expressed during its interactions with its host plant. These genes are distributed into eight well-defined expression clusters, corresponding to specific infection lifestyles or to tissue-specific genes. All expression clusters are enriched in effector genes, and one cluster is specific to the saprophytic lifestyle on plant residues. One cluster, including genes known to be involved in the first phase of asymptomatic fungal growth in leaves, is re-used at each asymptomatic growth stage, regardless of the type of organ infected. The expression of the genes of this cluster is repeatedly turned on and off during infection. Whatever their expression profile, the genes of these clusters are enriched in heterochromatin regions associated with H3K9me3 or H3K27me3 repressive marks. These findings provide support for the hypothesis that part of the fungal genes involved in niche adaptation is located in heterochromatic regions of the genome, conferring an extreme plasticity of expression. Conclusion This work opens up new avenues for plant disease control, by identifying stage-specific effectors that could be used as targets for the identification of novel durable disease resistance genes, or for the in-depth analysis of chromatin remodeling during plant infection, which could be manipulated to interfere with the global expression of effector genes at crucial stages of plant infection. Supplementary Information The online version contains supplementary material available at 10.1186/s12915-021-00989-3.

Published
2020

30. A new family of structurally conserved fungal effectors displays epistatic interactions with plant resistance proteins

Author

Lazar, Noureddine, primary, Mesarich, Carl H., additional, Petit-Houdenot, Yohann, additional, Talbi, Nacera, additional, de la Sierra-Gallay, Ines Li, additional, Zélie, Emilie, additional, Blondeau, Karine, additional, Gracy, Jérôme, additional, Ollivier, Bénédicte, additional, Blaise, Françoise, additional, Rouxel, Thierry, additional, Balesdent, Marie-Hélène, additional, Idnurm, Alexander, additional, van Tilbeurgh, Herman, additional, and Fudal, Isabelle, additional

Published
2020
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31. Origins of host-specific populations of the blast pathogen Magnaporthe oryzae in crop domestication with subsequent expansion of pandemic clones on rice and weeds of rice

Author

Couch, Brett C., Fudal, Isabelle, Lebrun, Marc-Henri, Tharreau, Didier, Valent, Barbara, van Kim, Pham, Notteghem, Jean-Loup, and Kohn, Linda M.

Subjects
Weeds -- Genetic aspects, Rice -- Genetic aspects, Genetic engineering, Crops, Cloning, Biological sciences
Abstract

Rice, as a widely and intensively cultivated crop, should be a target for parasite host shifts and a source for shifts to co-occurring weeds. Magnaporthe oryzae, of the M. grisea species complex, is the most important fungal pathogen of rice, with a high degree of host specificity. On the basis of 10 loci from six of its seven linkage groups, 37 multilocus haplotypes among 497 isolates of M. oryzae from rice and other grasses were identified. Phylogenetic relationships among isolates from rice (Oryza sativa), millet (Setaria spp.), cutgrass (Leersia hexandra), and torpedo grass (Panicum repens) were predominantly tree like, consistent with a lack of recombination, but from other hosts were reticulate, consistent with recombination. The single origin of rice-infecting M. oryzae followed a host shift from a Setaria millet and was closely followed by additional shifts to weeds of rice, cutgrass, and torpedo grass. Two independent estimators of divergence time indicate that these host shifts predate the Green Revolution and could be associated with rice domestication. The rice-infecting lineage is characterized by high copy number of the transposable element MGR586 (Pot3) and, except in two haplotypes, by a loss of AVR-Co39. Both mating types have been retained in ancestral, well-distributed rice-infecting haplotypes 10 (mainly temperate) and 14 (mainly tropical), but only one mating type was recovered from several derived, geographically restricted haplotypes. There is evidence of a common origin of both ACE1 virulence genotypes in haplotype 14. Host-haplotype association is evidenced by low pathogenicity on hosts associated with other haplotypes.

Published
2005

32. Large-scale transcriptomics to dissect two years of the life of a fungal phytopathogen interacting with its host plant

Author

Gay, Elise J., primary, Soyer, Jessica L., additional, Lapalu, Nicolas, additional, Linglin, Juliette, additional, Fudal, Isabelle, additional, Da Silva, Corinne, additional, Wincker, Patrick, additional, Aury, Jean-Marc, additional, Cruaud, Corinne, additional, Levrel, Anne, additional, Lemoine, Jocelyne, additional, Delourme, Regine, additional, Rouxel, Thierry, additional, and Balesdent, Marie-Hélène, additional

Published
2020
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36. Genome-wide histone map of the blackleg fungus Leptosphaeria maculans

Author

Soyer, Jessica, Clairet, Colin, GAY, Elise, Blaise, Francoise, Stukenbrock, Eva H., Fudal, Isabelle, BIOlogie et GEstion des Risques en agriculture (BIOGER), AgroParisTech-Institut National de la Recherche Agronomique (INRA), Université Paris Saclay (COMUE), Environmental Genomics Botanical Institute, Christian-Albrechts University of Kiel, Max Planck Institute for Evolutionary Biology, and Institut National de la Recherche Agronomique (INRA)-AgroParisTech

Subjects
epigenetique, effecteurs, [SDV]Life Sciences [q-bio], education, regulation, social sciences, health care economics and organizations
Abstract

Genome-wide histone map of the blackleg fungus Leptosphaeria maculans. 15th International Rapeseed Congress

Published
2019

37. Functional analysis of AvrLm10a and AvrLm10b two neighbor effector genes from L. maculans displaying a 'two genes for one gene' interaction with the resistance gene Rlm10 from Brassica nigra

Author

Petit, Yohann, Meyer, Michel, Blaise, Francoise, Ollivier, Benedicte, Marais, Claire-Line, Jauneau, Alain, Audran, Corinne, RIVAS, Susana, Rouxel, Thierry, Balesdent, Marie-Helene, Fudal, Isabelle, BIOlogie et GEstion des Risques en agriculture (BIOGER), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Université Paris Saclay (COmUE), Plateforme imagerie (PICTURES), IFR10, Laboratoire des interactions plantes micro-organismes (LIPM), and Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS)

Subjects
resistance, effecteurs, reconnaissance, [SDV]Life Sciences [q-bio], [SDE]Environmental Sciences, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, ComputingMilieux_MISCELLANEOUS, Avirulence
Abstract

International audience

Published
2019

38. Searching for resistance genes against Leptosphaeria maculans late effectors, involved in systemic colonization of Brassica napus

Author

JIQUEL, Audren, Gervais, Julie, Fudal, Isabelle, Pitarch, Anais, Fauré, S., Balesdent, Marie-Helene, Rouxel, Thierry, BIOlogie et GEstion des Risques en agriculture (BIOGER), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Université Paris Saclay (COmUE), and Euralis Semences

Subjects
transcriptomics, [SDV]Life Sciences [q-bio], fungus, Brassica napus, [SDE]Environmental Sciences, phytopathology, ComputingMilieux_MISCELLANEOUS, effectors
Abstract

International audience

Published
2019

40. Functional analysis of AvrLm10a and AvrLm10b two neighbor effector genes from L. maculans displaying a 'two genes for one gene' interaction with the resistance gene Rlm10 from Brassica nigra

Author

Petit, Yohann, Degrave, Alexandre, Meyer, Michel, Blaise, Francoise, Ollivier, Benedicte, Marais, Claire-Line, Jauneau, Alain, Audran, Corinne, RIVAS, Susana, Rouxel, Thierry, Balesdent, Marie-Helene, Fudal, Isabelle, BIOlogie et GEstion des Risques en agriculture (BIOGER), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Université Paris Saclay (COmUE), Plateforme imagerie (PICTURES), IFR10, Laboratoire des interactions plantes micro-organismes (LIPM), Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Fédération de Recherche Agrobiosciences, Interactions et Biodiversité (FR AIB), Université Toulouse III - Paul Sabatier (UT3), and Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)

Subjects
effecteurs, avirulence, resistance, relation gene-pour-gene, colza, Leptosphaeria maculans, Effecteurs, reconnaissance, [SDV]Life Sciences [q-bio], [SDE]Environmental Sciences, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, résistance, ComputingMilieux_MISCELLANEOUS, Avirulence
Abstract

National audience

Published
2018

41. Deciphering the involvement of an effector family from the plant pathogenic fungus Leptosphaeria maculans in oilseed rape infection

Author

TALBI, Nacera, Petit, Yohann, Marais, Claire-Line, Ollivier, Benedicte, Blaise, Francoise, Rouxel, Thierry, Balesdent, Marie-Helene, Fudal, Isabelle, BIOlogie et GEstion des Risques en agriculture (BIOGER), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, and Université Paris Saclay (COmUE)

Subjects
Effecteurs, [SDV]Life Sciences [q-bio], [SDE]Environmental Sciences, résistance, pathogénie, avirulence, ComputingMilieux_MISCELLANEOUS
Abstract

National audience

Published
2018

42. Investigating the involvement of histone modifications in the control of effector gene expression in Leptospharia maculans, the fungus causing stem canker of oilseed rape

Author

Soyer, Jessica L, Fudal, Isabelle, Clairet, Colin, Lapalu, Nicolas, Simon, Adeline, Blaise, Francoise, Stukenbrock, Eva H., BIOlogie et GEstion des Risques en agriculture (BIOGER), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Université Paris Saclay (COmUE), Max Planck Institute for Evolutionary Biology, Max-Planck-Gesellschaft, and Christian-Albrechts University of Kiel

Subjects
ChIP-seq, Leptosphaeria maculans, [SDV]Life Sciences [q-bio], [SDE]Environmental Sciences, regulation, MAINE-seq, ComputingMilieux_MISCELLANEOUS, effectors
Abstract

National audience

Published
2018

43. Investigating the involvement of the chromatin state in the control of effector gene expression in Leptosphaeria maculans

Author

Clairet, Colin, Soyer, Jessica L., Lapalu, Nicolas, Simon, Adeline, Blaise, Francoise, Gervais, Julie, Stukenbrock, Eva H., Fudal, Isabelle, BIOlogie et GEstion des Risques en agriculture (BIOGER), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Université Paris Saclay (COmUE), Max Planck Institute for Evolutionary Biology, Max-Planck-Gesellschaft, and Christian-Albrechts University of Kiel

Subjects
Leptosphaeria maculans, effecteurs, [SDV]Life Sciences [q-bio], [SDE]Environmental Sciences, regulation, chromatine, colza, ComputingMilieux_MISCELLANEOUS
Abstract

National audience

Published
2018

44. Identification et analyse fonctionnelle des effecteurs tardifs impliqués dans la colonisation systémique du colza par Leptosphaeria maculans

Author

Gervais, Julie, Gay, Elise, Dutreux, Fabien, Fudal, Isabelle, LINGLIN, Juliette, Ollivier, Benedicte, Aury, Jean-Marc, Balesdent, Marie-Helene, Rouxel, Thierry, BIOlogie et GEstion des Risques en agriculture (BIOGER), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Université Paris Saclay (COmUE), and Bayer Cropscience

Subjects
nécrose du collet, gène-pour-gène, Colza, RNAseq, [SDV]Life Sciences [q-bio], [SDE]Environmental Sciences, ComputingMilieux_MISCELLANEOUS
Abstract

National audience

Published
2018

45. Structural and functional characterization of Leptosphaeria maculans effectors: the example of AvrLm4-7

Author

Petit, Yohann, Blaise, Francoise, Plissonneau, Clémence, Rouxel, Thierry, Balesdent, Marie-Helene, Blondeau, Karine, Noureddine, Lazar, Gallay, Inès, Le Moigne, Théo, Van Tilbeurgh, Herman, Fudal, Isabelle, BIOlogie et GEstion des Risques en agriculture (BIOGER), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Fonction et Architecture des Assemblages Macromoléculaires (FAAM), Département Biochimie, Biophysique et Biologie Structurale (B3S), Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), AgroParisTech-Institut National de la Recherche Agronomique (INRA), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Institut de Biologie Intégrative de la Cellule (I2BC), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), BIOlogie GEstion des Risques en agriculture - Champignons Pathogènes des Plantes ( BIOGER-CPP ), Institut National de la Recherche Agronomique ( INRA ) -AgroParisTech, Fonction et Architecture des Assemblages Macromoléculaires ( FAAM ), Département Biochimie, Biophysique et Biologie Structurale ( B3S ), Institut de Biologie Intégrative de la Cellule ( I2BC ), Université Paris-Saclay-Centre National de la Recherche Scientifique ( CNRS ) -Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Université Paris-Sud - Paris 11 ( UP11 ) -Université Paris-Saclay-Centre National de la Recherche Scientifique ( CNRS ) -Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Université Paris-Sud - Paris 11 ( UP11 ) -Institut de Biologie Intégrative de la Cellule ( I2BC ), and Université Paris-Saclay-Centre National de la Recherche Scientifique ( CNRS ) -Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Université Paris-Sud - Paris 11 ( UP11 ) -Université Paris-Saclay-Centre National de la Recherche Scientifique ( CNRS ) -Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Université Paris-Sud - Paris 11 ( UP11 )

Subjects
[ SDV ] Life Sciences [q-bio], avirulence gene, pathogenesis, [SDV]Life Sciences [q-bio], stem canker, effectors
Abstract

During plant infection, pathogens secrete an arsenal of effectors, key elements of pathogenesis which modulate innate immunity of the plant and facilitate infection. Fungal effector genes typically encode small proteins, predicted to be secreted, with no homology in databases, and absence of known motif. As such their function or role in pathogenesis is mostly unknown. The phytopathogenic ascomycete Leptosphaeria maculans is the causal agent of stem canker of oilseed rape. More than 650 putative effector-encoding genes have been identified in its genome, 7 of them corresponding to avirulence proteins. We develop a project aiming at elucidating the involvement of L. maculans effectors in pathogenicity through the structural and functional characterization of a few major effector proteins and the determination of their interactants. Our strategy is illustrated here with AvrLm4-7, a 143 amino-acid long secreted protein important for fungal fitness and recognized by two oilseed rape resistance proteins, Rlm4 and Rlm7. One single amino-acid change is sufficient to lose recognition by Rlm4 while maintaining recognition by Rlm7. 3D-structure of an isoform of AvrLm4-7 only recognized by Rlm7 was previously determined, allowing us to define regions implicated in recognition by Rlm7 and translocation into plant cell. We recently determined the 3D-structure of another isoform of AvrLm4-7 recognized both by Rlm4 and Rlm7, showing that the amino-acid change allowing to escape Rlm4-recognition was located on an external loop and did not change the overall structure of the protein. AvrLm4-7 was also recently shown to suppress recognition of another L. maculans avirulence gene, AvrLm3, by its cognate resistance gene Rlm3, leading us to hypothesize a suppression of Effector-Triggered Immunity (ETI) by AvrLm4-7. In order to test that hypothesis, we transiently expressed AvrLm4-7 and several cell-death inducers in Nicotiana benthamiana epidermal cells: AvrLm4-7 was able to suppress cell death induced by BAX and AvrPto. We also generated transgenic lines of Arabidopsis thaliana constitutively expressing AvrLm4-7 and are currently characterizing the lines for their susceptibility to pathogens with contrasted lifestyles and for their ability to suppress recognition of Pseudomonas syringae avirulence proteins. A better understanding of the role of an effector implicated in the masking of another effector will allow us to develop alternative strategies to genetically control stem canker disease.

Published
2017

46. Leptosphaeria maculans effectors involved in the oilseed rape systemic colonization

Author

Gervais, Julie, Plissonneau, Clémence, LINGLIN, Juliette, Meyer, Michel, Labadie, K, Cruaud, Corinne, Ollivier, Benedicte, Fudal, Isabelle, Rouxel, Thierry, Balesdent, Marie-Helene, BIOlogie et GEstion des Risques en agriculture (BIOGER), AgroParisTech-Institut National de la Recherche Agronomique (INRA), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), AGROCAMPUS OUEST-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National de la Recherche Agronomique (INRA), URM 1290 BIOGR, Université Paris-Saclay, Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, and Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)

Subjects
chancre de la tige, oilseed rape, colonisation, [SDV]Life Sciences [q-bio], food and beverages, colza, stem canker
Abstract

The stem canker disease, caused by Leptosphaeria maculans, is one of the most devastating diseases of oilseed rape (canola). It colonizes the plant in two stages: a short and early colonisation stage corresponding to cotyledon or leaf colonisation, and a late colonisation stage during which the fungus colonises systemically and symptomlessly the plant during several months before stem canker appears. To date, determinants of the late colonisation stage remain poorly understood. By a transcriptomic approach, we previously identified two waves of effector candidate expression during the early and late colonisation stages (Gervais et al, 2016). The late effector candidates are located in gene-rich genomic regions, whereas the early effector genes are located in gene-poor regions of the genome. Among the late effector candidates identified, we selected 6 genes for further characterization. We created mutants silenced for these effector candidates. For one of these genes, its expression level correlated negatively with the size of the necrosis observed in the stem. The identification of new effector genes would contribute to the identification of new resistance genes specific to these effectors. To easily identify matching resistance genes in oilseed rape, we created transgenic isolates expressing these 6 late effectors at the early steps of infection to provide medium-throughput strategies to screen more efficiently different cultivars. Preliminary results indicate that some cultivars with adult resistance were more resistant to these transgenic isolates in cotyledon assays. With this approach, we also identified a cultivar carrying a specific resistance to one these 6 effector candidates. Reference Gervais, J., Plissonneau, C., Linglin, J., Meyer, M., Labadie, K., Cruaud, C., Fudal, I., Rouxel, T. and Balesdent, M.H. (2016) Different waves of effector genes with contrasted genomic location are expressed by Leptosphaeria maculans during cotyledon and stem colonization of oilseed rape. Mol. Plant Pathol.

Published
2017

47. Influence of histone modifications on effector gene expression in the plant pathogenic fungus Leptosphaeria maculans

Author

Soyer, Jessica, Clairet, Colin, Gervais, Julie, Balesdent, Marie-Helene, Connolly, Lanelle R, Freitag, Michael, Rouxel, Thierry, Fudal, Isabelle, BIOlogie et GEstion des Risques en agriculture (BIOGER), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Center for Genome Research and Biocomputing, Department of Biochemistry and Biophysics, Oregon State University (OSU), Ruhr-Universität Bochum [Bochum], and AgroParisTech-Institut National de la Recherche Agronomique (INRA)

Subjects
Leptosphaeria maculans, gene-rich, [SDV]Life Sciences [q-bio], Brassica napus, gene-poor, genome
Abstract

Leptosphaeria maculans, the fungus responsible for stem canker of oilseed rape (Brassica napus), presents a particular genome structure divided into gene-rich and transposable element (TE)-rich regions. The latter are proposed to be heterochromatic domains, as they are gene-poor, TE-rich and present lower recombination rates than gene-rich regions. While overall gene-poor, TE-rich regions are enriched for putative effector genes specifically expressed during the early stages of plant infection (‘early’ effector genes). In contrast, effector genes expressed during the late stages of infection (endophytic growth and stem necrosis, ‘late’ effector genes) are located in gene-rich regions. We investigated the concerted expression of ‘early’ effector genes by assessing whether TE-rich regions could be targets of reversible chromatin modifications that affect the regulation of effector gene expression. We first examined the involvement of one histone modification, histone H3 lysine 9 tri-methylation (H3K9me3) in chromatin-based regulation of effector gene expression. For this purpose, we silenced expression of two key players in heterochromatin assembly and maintenance, HP1 and KMT1, by RNAi. Silencing of HP1 and KMT1 led to an over-expression of ‘early’ effector genes in TE-rich regions during in vitro growth (but no induction of ‘late’ effector gene expression). The increase of expression was associated with a reduction of H3K9 tri-methylation at two effector-encoding gene loci. Our data strongly suggest that a chromatin-based control, mediated by HP1 and KMT1, represses the expression of at least part of the ‘early’ effector genes located in TE-rich regions during growth in axenic culture. We are currently investigating the role of another key player in heterochromatin assembly, KMT6, involved in the heterochromatic-associated histone modification H3K27me3, on the control of effector gene expression

Published
2017

48. In planta localisation of Leptosphaeria maculans effectors and identification of their plant targets

Author

Marais, Claire-Line, Petit, Yohann, Blaise, Francoise, Ollivier, Benedicte, Gervais, Julie, Le Moigne,, Rouxel, Thierry, Balesdent, Marie-Helene, Gallay, Inès, Blondeau, K, Lazar, Noureddine, Van Tilbeurgh, Herman, Fudal, Isabelle, BIOlogie et GEstion des Risques en agriculture (BIOGER), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Swiss Federal Institute of Technology, and Centre National de la Recherche Scientifique (CNRS)

Subjects
effector, fungal, pathogenesis, [SDV]Life Sciences [q-bio], [SDE]Environmental Sciences, genes
Abstract

International audience; Fungal effector genes are very diverse and typically encode small proteins, predicted to be secreted, with no or low homology in databases, and absence of known motif. As such their function or role in pathogenesis is mostly unknown. On these bases, the StructuraLEP project aims at elucidating the involvement of L. maculans effectors in pathogenicity through the structural and functional characterization of a few major effector proteins and the determination of their interactants. We are investigating six L. maculans effectors chosen for their biological significance (involvement in fungal fitness, cognate R gene identified) or because they may represent novel modes of interaction with their plant target (two AVR genes have to be recognized by a specific R gene). We present here the strategies developed within the project to answer two questions: (i) “Where do L. maculans effectors act during plant infection?” and (ii) “Which proteins interact with L. maculans effectors?”. In order to localise L. maculans effectors into plant cells and to identify their plant targets, we will transiently express effectors with a fluorescent tag into tobacco leaf epidermal cells and observe effector localisation by confocal microscopy. Tobacco leaves expressing effectors will be used to perform pull-down assays and tobacco proteins interacting with effectors will be identified through mass spectrometry. A more exploratory but biologically relevant strategy will also be tested. L. maculans transformants stably expressing effectors with HA-tag will be used to infect oilseed rape leaves. Localisation of effectors in oilseed rape leaves will be performed by immunocytolocalisation using antibodies against the HA-tag. The infected oilseed rape leaves will also be used to perform pull-down assays in order to identify plant proteins targeted by L. maculans effectors.

Published
2017

49. Chromatin-based control of plant-fungi interactions

Author

Fudal, Isabelle, BIOlogie et GEstion des Risques en agriculture (BIOGER), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, and Université Paris Saclay (COmUE)

Subjects
'plastic', [SDV]Life Sciences [q-bio], [SDE]Environmental Sciences, fungi, genomic regions, colonization, effectors
Abstract

International audience; Plant pathogens, including plant-associated fungi, secrete during plant infection an arsenal of small secreted proteins acting as effectors that modulate host immunity to facilitate infection. Genome-wide transcriptomic studies have shown waves of concerted expression of effector genes that correspond to different stages of plant tissue infection and colonization. In parallel, effector genes were often found to be located in ‘plastic’ genomic regions, enriched in transposable elements. The location of effector genes in regions enriched in transposable elements has been shown to have an impact on adaptability of fungi but could also provide for tight control of effector gene expression through chromatin-based regulation. Recently, chromatin structure was shown to be an important regulatory layer of effector gene expression in several plant-associated fungi with different lifestyles. Chromatin-based control of effector gene expression is likely to provide an evolutionary advantage by preventing the expression of genes not needed during vegetative growth and allow for a massive concerted expression at particular time-points of plant infection.

Published
2017

50. Different waves of effector genes with contrasted genomic location are expressed by Leptosphaeria maculans during cotyledon and stem colonization of oilseed rape

Author

Gervais, Julie, Plissonneau, Clémence, LINGLIN, Juliette, Meyer, Michel, Labadie, Karine, Cruaud, Corinne, Fudal, Isabelle, Rouxel, Thierry, Balesdent, Marie-Helene, BIOlogie et GEstion des Risques en agriculture (BIOGER), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), ONEMA-CTPS : 'ICOSCOP', INRA-SMaCH Metaprogram 'K-Masstec', France Génomique 'LEPTOLIFE', Terres Inovia, and AgroParisTech-Institut National de la Recherche Agronomique (INRA)

Subjects
Leptosphaeria maculans, Plant Stems, Sequence Analysis, RNA, Gene Expression Profiling, [SDV]Life Sciences [q-bio], Genes, Fungal, Brassica napus, effector waves, Colony Count, Microbial, Down-Regulation, Reproducibility of Results, food and beverages, RNA sequencing, Original Articles, Up-Regulation, isochores, transcriptomics, Gene Ontology, Ascomycota, Gene Expression Regulation, Fungal, RNA, Messenger, Cotyledon
Abstract

Leptosphaeria maculans, the causal agent of stem canker disease, colonizes oilseed rape (Brassica napus) in two stages: a short and early colonization stage corresponding to cotyledon or leaf colonization, and a late colonization stage during which the fungus colonizes systemically and symptomlessly the plant during several months before stem canker appears. To date, the determinants of the late colonization stage are poorly understood; L. maculans may either successfully escape plant defences, leading to stem canker development, or the plant may develop an ‘adult‐stage’ resistance reducing canker incidence. To obtain an insight into these determinants, we performed an RNA‐sequencing (RNA‐seq) pilot project comparing fungal gene expression in infected cotyledons and in symptomless or necrotic stems. Despite the low fraction of fungal material in infected stems, sufficient fungal transcripts were detected and a large number of fungal genes were expressed, thus validating the feasibility of the approach. Our analysis showed that all avirulence genes previously identified are under‐expressed during stem colonization compared with cotyledon colonization. A validation RNA‐seq experiment was then performed to investigate the expression of candidate effector genes during systemic colonization. Three hundred and seven ‘late’ effector candidates, under‐expressed in the early colonization stage and over‐expressed in the infected stems, were identified. Finally, our analysis revealed a link between the regulation of expression of effectors and their genomic location: the ‘late’ effector candidates, putatively involved in systemic colonization, are located in gene‐rich genomic regions, whereas the ‘early’ effector genes, over‐expressed in the early colonization stage, are located in gene‐poor regions of the genome.

Published
2017

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