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1. Understanding human fetal pancreas development using subpopulation sorting, RNA sequencing and single-cell profiling

Author

Nicolas Glaser, Nicola L. Beer, Martijn van de Bunt, Cyrille Ramond, Mark I. McCarthy, Christian Honoré, Raphael Scharfmann, Claire Berthault, Belin Selcen Beydag-Tasöz, Anne Grapin-Botton, Ajuna Azad, Mattias Hansson, Maja Borup Kjær Petersen, and Anna L. Gloyn

Subjects
0301 basic medicine, Pluripotent Stem Cells, Transcription, Genetic, Human Development, Enteroendocrine cell, Computational biology, Biology, Transcriptome, 03 medical and health sciences, 0302 clinical medicine, Fetus, medicine, Gene family, Humans, Progenitor cell, Induced pluripotent stem cell, Molecular Biology, Pancreas, Gene Expression Profiling, Gene Expression Regulation, Developmental, Flow Cytometry, Gene expression profiling, 030104 developmental biology, medicine.anatomical_structure, Stem cell, 030217 neurology & neurosurgery, Developmental Biology
Abstract

To decipher the populations of cells present in the human fetal pancreas and their lineage relationships, we developed strategies to isolate pancreatic progenitors, endocrine progenitors and endocrine cells. Transcriptome analysis of the individual populations revealed a large degree of conservation among vertebrates in the drivers of gene expression changes occurring at different steps of differentiation, although notably, sometimes, different members of the same gene family are expressed. The transcriptome analysis establishes a resource to identify novel genes and pathways involved in human pancreas development. Single cell profiling further captured intermediate stages of differentiation and enabled us to decipher the sequence of transcriptional events occurring during human endocrine differentiation. Furthermore, we evaluate how well individual pancreatic cells derived in vitro from human pluripotent stem cells mirror the natural process occurring in human fetuses. This comparison uncovers a few differences at the progenitor steps, a convergence at the steps of endocrine induction and the current inability to fully resolve endocrine cell subtypes in vitro.

Published
2018

3. Priming 3D Cultures of Human Mesenchymal Stromal Cells Toward Cartilage Formation Via Developmental Pathways

Author

Stefan Schären, Matteo Centola, Beatrice Tonnarelli, Nicolas Glaser, Ivan Martin, and Andrea Barbero

Subjects
Adult, Male, Stromal cell, Cellular differentiation, Cell Culture Techniques, Gene Expression, Bone Marrow Cells, Cartilage metabolism, Biology, Fibroblast growth factor, 03 medical and health sciences, Chondrocytes, 0302 clinical medicine, Original Research Reports, Wnt3A Protein, Humans, Limb development, Wnt Signaling Pathway, Cells, Cultured, Cell Proliferation, 030304 developmental biology, 0303 health sciences, Reverse Transcriptase Polymerase Chain Reaction, Mesenchymal stem cell, Cell Differentiation, Mesenchymal Stem Cells, Cell Biology, Hematology, Flow Cytometry, Molecular biology, 3. Good health, Cell biology, Cartilage, Microscopy, Fluorescence, Cell culture, 030220 oncology & carcinogenesis, Female, Fibroblast Growth Factor 2, Stem cell, Chondrogenesis, Signal Transduction, Developmental Biology
Abstract

The field of regenerative medicine has increasingly recognized the importance to be inspired by developmental processes to identify signaling pathways crucial for 3D organogenesis and tissue regeneration. Here, we aimed at recapitulating the first events occurring during limb development (ie, cell condensation and expansion of an undifferentiated mesenchymal cell population) to prime 3D cultures of human bone marrow-derived mesenchymal stromal/stem cells (hBM-MSC) toward the chondrogenic route. Based on embryonic development studies, we hypothesized that Wnt3a and fibroblast growth factor 2 (FGF2) induce hBM-MSC to proliferate in 3D culture as an undifferentiated pool of progenitors (defined by clonogenic capacity and expression of typical markers), retaining chondrogenic potential upon induction by suitable morphogens. hBM-MSC were responsive to Wnt signaling in 3D pellet culture, as assessed by significant upregulation of main target genes and increase of unphosphorylated β-catenin levels. Wnt3a was able to induce a five-fold increase in the number of proliferating hBM-MSC (6.4% vs. 1.3% in the vehicle condition), although total DNA content of the 3D construct was decreasing over time. Preconditioning with Wnt3a improved transforming growth factor-β1 mediated chondrogenesis (30% more glycosaminoglycans/cell in average). In contrast to developmental and 2D MSC culture models, FGF2 antagonized the Wnt-mediated effects. Interestingly, the CD146+ subpopulation was found to be more responsive to Wnt3a. The presented data indicate a possible strategy to prime 3D cultures of hBM-MSC by invoking a “developmental engineering” approach. The study also identifies some opportunities and challenges to cross-fertilize skeletal development models and 3D hBM-MSC culture systems.

Published
2013

4. Mutations in BOREALIN cause thyroid dysgenesis

Author

Athanasia Stoupa, Claude Besmond, Cyrille Ramond, Delphine Zenaty, Raphael Scharfmann, Christine Bole-Feysot, Dulanjalee Kariyawasam, William R. Taylor, Arnold Munnich, Sébastien Gaujoux, Laurence Hubert, Juliane Léger, Taylor M Monus, Patrick Nitschke, Nicolas Glaser, Frédéric Sebag, Aurore Carré, Michel Polak, Stanislas Lyonnet, and Manelle Gueriouz

Subjects
0301 basic medicine, medicine.medical_specialty, Mutation, Missense, Mitosis, Cell Cycle Proteins, Biology, medicine.disease_cause, Thyroid dysgenesis, 03 medical and health sciences, Cell Movement, Internal medicine, Genetics, medicine, Missense mutation, Humans, Exome, Genetic Predisposition to Disease, Molecular Biology, Gene, Genetics (clinical), Exome sequencing, Mutation, Thyroid, High-Throughput Nucleotide Sequencing, General Medicine, Articles, medicine.disease, Congenital hypothyroidism, Pedigree, 030104 developmental biology, Endocrinology, medicine.anatomical_structure, Gene Expression Regulation, Thyroid Dysgenesis, Female, PAX8
Abstract

Congenital hypothyroidism is the most common neonatal endocrine disorder and is primarily caused by developmental abnormalities otherwise known as thyroid dysgenesis (TD). We performed whole exome sequencing (WES) in a consanguineous family with TD and subsequently sequenced a cohort of 134 probands with TD to identify genetic factors predisposing to the disease. We identified the novel missense mutations p.S148F, p.R114Q and p.L177W in the BOREALIN gene in TD-affected families. Borealin is a major component of the Chromosomal Passenger Complex (CPC) with well-known functions in mitosis. Further analysis of the missense mutations showed no apparent effects on mitosis. In contrast, expression of the mutants in human thyrocytes resulted in defects in adhesion and migration with corresponding changes in gene expression suggesting others functions for this mitotic protein. These results were well correlated with the same gene expression pattern analysed in the thyroid tissue of the patient with BOREALIN-p.R114W. These studies open new avenues in the genetics of TD in humans.

Published
2016

5. Differential expression of the chemosensory transcriptome in two populations of the stemborer Sesamia nonagrioides

Author

Fabrice Legeai, Aurore Gallot, Emmanuelle Jacquin-Joly, Paul-André Calatayud, Bruno Le Ru, Myriam Harry, Nicolas Glaser, Laure Kaiser, Institut d'écologie et des sciences de l'environnement de Paris (iEES), Centre National de la Recherche Scientifique (CNRS)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Recherche Agronomique (INRA), Évolution, génomes, comportement et écologie (EGCE), Centre National de la Recherche Scientifique (CNRS)-IRD-Université Paris-Sud - Paris 11 (UP11), Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-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 la Recherche Agronomique (INRA)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Centre National de la Recherche Scientifique (CNRS), Université Paris-Sud - Paris 11 (UP11)-IRD-Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Institut d'écologie et des sciences de l'environnement de Paris (IEES), Scalable, Optimized and Parallel Algorithms for Genomics (GenScale), GESTION DES DONNÉES ET DE LA CONNAISSANCE (IRISA-D7), Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Université de Bretagne Sud (UBS)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-Télécom Bretagne-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-CentraleSupélec-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Université de Rennes (UNIV-RENNES)-CentraleSupélec-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Université de Rennes (UNIV-RENNES)-CentraleSupélec-Inria Rennes – Bretagne Atlantique, Institut National de Recherche en Informatique et en Automatique (Inria), Evolution, adaptation et comportement, Département écologie évolutive [LBBE], Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), International Centre of Insect Physiology and Ecology (ICIPE), and ICIPE

Subjects
Arthropod Antennae, Oviposition, media_common.quotation_subject, [SDV]Life Sciences [q-bio], Population, Sesamia nonagrioides, Genes, Insect, Insect, Moths, Typhaceae, Zea mays, Biochemistry, Transcriptome, Cytochrome P-450 Enzyme System, medicine, Animals, Adaptation, education, Molecular Biology, media_common, Local adaptation, education.field_of_study, Olfactory receptor, biology, Ecology, Gene Expression Profiling, fungi, biology.organism_classification, RNAseq, Adaptation, Physiological, Kenya, Smell, Gene expression profiling, medicine.anatomical_structure, Evolutionary biology, Larva, Insect Science, Female, Chemosensory genes, France, [INFO.INFO-BI]Computer Science [cs]/Bioinformatics [q-bio.QM]
Abstract

International audience; Among the proposed mechanisms of local adaptation to different ecological environments, transcriptional changes may play an important role. In this study, we investigated whether such variability occurred within the chemosensory organs of a herbivorous insect, for which chemosensation guides most of its host preferences. A European and an African population of the noctuid Sesamia nonagrioides that display significant differences in their ecological preferences were collected on Zea mays and Typha domingensis, respectively. RNAseq were used between the two populations for digital expression profiling of chemosensory organs from larval antennae and palps. Preliminary data on adult female antennae and ovipositors were also collected. We found 6,550 differentially expressed transcripts in larval antennae and palps. Gene ontology enrichment analyses suggested that transcriptional activity was overrepresented in the French population and that virus and defense activities were overrepresented in the Kenyan population. In addition, we found differential expression of a variety of cytochrome P450s, which may be linked to the different host-plant diets. Looking at olfactory genes, we observed differential expression of numerous candidate odorant-binding proteins, chemosensory proteins, and one olfactory receptor, suggesting that differences in olfactory sensitivity participate in insect adaptation.

Published
2015
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6. Similar Differentiation Patterns Between PBP Expression Levels and Pheromone Component Ratios in Two Populations of Sesamia nonagrioides

Author

Thomas Lecocq, Ene Leppik, Myriam Harry, Christelle Monsempes, Claire Capdevielle-Dulac, Brigitte Frérot, Bruno Le Ru, Nicolas Glaser, Emmanuelle Jacquin-Joly, Paul-André Calatayud, Physiologie de l'Insecte, Signalisation et Communication [Versailles] (PISC), Institut National de la Recherche Agronomique (INRA), Institut d'écologie et des sciences de l'environnement de Paris (iEES), Centre National de la Recherche Scientifique (CNRS)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Recherche Agronomique (INRA), Physiologie de l'Insecte : Signalisation et Communication (PISC), Institut National de la Recherche Agronomique (INRA)-Université Pierre et Marie Curie - Paris 6 (UPMC)-AgroParisTech, Université Paris Sud (Paris 11), UMR Lab Evolut. Genomes Speciat., Institut de Recherche pour le Développement (IRD [France-Ouest]), Unité de Recherches Animal et Fonctionnalités des Produits Animaux (URAFPA), Université de Lorraine (UL)-Institut National de la Recherche Agronomique (INRA), Laboratoire de Zoologie [Mons], University of Mons [Belgium] (UMONS), Évolution, génomes, comportement et écologie (EGCE), Centre National de la Recherche Scientifique (CNRS)-IRD-Université Paris-Sud - Paris 11 (UP11), French ANR (Agence Nationale de la Recherche) [ANR-09-PEXT-009], Institut d'écologie et des sciences de l'environnement de Paris (IEES), Institut National de la Recherche Agronomique (INRA)-Université de Lorraine (UL), Université Paris-Sud - Paris 11 (UP11)-IRD-Centre National de la Recherche Scientifique (CNRS), and Institut National de la Recherche Agronomique (INRA)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Male, Sex pheromones, Pheromone-binding proteins, Population, Sesamia nonagrioides, Gene Expression, Moths, Real-Time Polymerase Chain Reaction, Biochemistry, Lepidoptera genitalia, Quantitative PCR, Stemborer, Botany, polycyclic compounds, Animals, Differential expression, Sex Attractants, education, Ecology, Evolution, Behavior and Systematics, Phylogeny, Genetics, education.field_of_study, biology, Geography, General Medicine, biology.organism_classification, Kenya, Lepidoptera, [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, Noctuidae, Sex pheromone, Pheromone, Insect Proteins, Female, France, Carrier Proteins
Abstract

International audience; Pheromone-binding proteins (PBPs) are thought to contribute to the specificity of the pheromone detection system through an initial selective binding with pheromone molecules. Here, we report different expression levels of PBP transcripts in the antennae of two populations of the stemborer Sesamia nonagrioides (Lepidoptera: Noctuidae), one collected in Europe and one in sub-Saharan Africa. The three PBP transcripts previously identified in this species were found to be expressed in both male and female antennae. Whereas PBP3 did not show any differential expression, PBP1 and PBP2 appeared to be expressed differently according to the population origin and sex. Simultaneously, we measured and compared the ratio of the three components of the S. nonagrioides pheromone blend (Z11-16:Ac; Z11-16:OH; Z11-16:Ald) in females of the two populations. The ratio of Z11-16:OH and Z11-16:Ald varied significantly according to the population origin of this species. Cluster analyses revealed similar differentiation patterns between PBP1 and PBP2 expression levels and the ratios of Z11-16:OH and Z11-16:Ald. Different female sexual signals may thus correspond to different male reception systems, which are adjusted by the PBP expression levels, thereby ensuring optimal communication within populations.

Published
2014
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7. A Comparison of the Olfactory Gene Repertoires of Adults and Larvae in the Noctuid Moth Spodoptera littoralis

Author

Nicolas Montagné, Fabrice Legeai, Erwan Poivet, Aurore Gallot, Emmanuelle Jacquin-Joly, Nicolas Glaser, Physiologie de l'Insecte : Signalisation et Communication (PISC), Institut National de la Recherche Agronomique (INRA)-Université Pierre et Marie Curie - Paris 6 (UPMC)-AgroParisTech, Evolution, adaptation et comportement, Département écologie évolutive [LBBE], Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Laboratoire Navier (navier umr 8205), Institut Français des Sciences et Technologies des Transports, de l'Aménagement et des Réseaux (IFSTTAR)-École des Ponts ParisTech (ENPC)-Centre National de la Recherche Scientifique (CNRS), Physiologie de l'Insecte, Signalisation et Communication [Versailles] (PISC), Institut National de la Recherche Agronomique (INRA), Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Institut National de la Recherche Agronomique (INRA)-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), Scalable, Optimized and Parallel Algorithms for Genomics (GenScale), GESTION DES DONNÉES ET DE LA CONNAISSANCE (IRISA-D7), Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), CentraleSupélec-Télécom Bretagne-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National de Recherche en Informatique et en Automatique (Inria)-École normale supérieure - Rennes (ENS Rennes)-Université de Bretagne Sud (UBS)-Centre National de la Recherche Scientifique (CNRS)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-CentraleSupélec-Télécom Bretagne-Université de Rennes 1 (UR1), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Inria Rennes – Bretagne Atlantique, Institut National de Recherche en Informatique et en Automatique (Inria), AGROCAMPUS OUEST-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National de la Recherche Agronomique (INRA), Inria Rennes – Bretagne Atlantique, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-GESTION DES DONNÉES ET DE LA CONNAISSANCE (IRISA-D7), Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-Télécom Bretagne-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-Télécom Bretagne-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Télécom Bretagne-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-Télécom Bretagne-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-Télécom Bretagne-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), and Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Télécom Bretagne-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)

Subjects
Male, Gene Expression, Genes, Insect, Insect, anophèles gambiae, Transcriptomes, Transcriptome, 0302 clinical medicine, Morphogenesis, Cluster Analysis, media_common, Genetics, Heliothis-Virescens, 0303 health sciences, Larva, Multidisciplinary, Ecology, Odorant-Binding-Protein, Manduca-Sexta, Genomics, Multiple Sequence Alignment, [SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], Sensory Systems, Smell, Medicine, Pheromone, Female, récepteur, Research Article, phéromone sexuelle, Arthropod Antennae, Science, media_common.quotation_subject, Chemosensory Proteins, Spodoptera, Biology, Sex-Pheromone Receptor, bombyx mori, 03 medical and health sciences, Genome Analysis Tools, Botany, Animals, Caterpillar, Spodoptera littoralis, Ionotropic Glutamate Receptors, Gene, 030304 developmental biology, Mosquito Anopheles-Gambiae, Olfactory System, Chemical Ecology, Expression Pattern, Bombyx-Mori, Gene Expression Profiling, fungi, Computational Biology, Molecular Sequence Annotation, Olfactory Perception, biology.organism_classification, heliothis virescens, Gene expression profiling, [INFO.INFO-BI]Computer Science [cs]/Bioinformatics [q-bio.QM], [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Zoology, Entomology, 030217 neurology & neurosurgery, Developmental Biology, Neuroscience
Abstract

International audience; To better understand the olfactory mechanisms in a lepidopteran pest model species, the cotton leafworm Spodoptera littoralis, we have recently established a partial transcriptome from adult antennae. Here, we completed this transcriptome using next generation sequencing technologies, namely 454 and Illumina, on both adult antennae and larval tissues, including caterpillar antennae and maxillary palps. All sequences were assembled in 77,643 contigs. Their analysis greatly enriched the repertoire of chemosensory genes in this species, with a total of 57 candidate odorant-binding and chemosensory proteins, 47 olfactory receptors, 6 gustatory receptors and 17 ionotropic receptors. Using RT-PCR, we conducted the first exhaustive comparison of olfactory gene expression between larvae and adults in a lepidopteran species. All the 127 candidate olfactory genes were profiled for expression in male and female adult antennae and in caterpillar antennae and maxillary palps. We found that caterpillars expressed a smaller set of olfactory genes than adults, with a large overlap between these two developmental stages. Two binding proteins appeared to be larvae-specific and two others were adult-specific. Interestingly, comparison between caterpillar antennae and maxillary palps revealed numerous organ-specific transcripts, suggesting the complementary involvement of these two organs in larval chemosensory detection. Adult males and females shared the same set of olfactory transcripts, except two male-specific candidate pheromone receptors, two male-specific and two female-specific odorant-binding proteins. This study identified transcripts that may be important for sex-specific or developmental stage-specific chemosensory behaviors.

Published
2013
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8. Candidate chemosensory genes in the Stemborer Sesamia nonagrioides

Author

Paul-André Calatayud, Myriam Harry, Erwan Poivet, Nicolas Montagné, Fabrice Legeai, Aurore Gallot, Emmanuelle Jacquin-Joly, Nicolas Glaser, Physiologie de l'Insecte, Signalisation et Communication [Versailles] (PISC), Institut National de la Recherche Agronomique (INRA), Laboratoire Evolution, Génomes et Spéciation [Gif-sur-Yvette] (LEGS), Institut de recherche pour le développement [IRD] : UR072-Centre National de la Recherche Scientifique (CNRS), Scalable, Optimized and Parallel Algorithms for Genomics (GenScale), Inria Rennes – Bretagne Atlantique, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-GESTION DES DONNÉES ET DE LA CONNAISSANCE (IRISA-D7), Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-Télécom Bretagne-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-Télécom Bretagne-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Télécom Bretagne-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS), Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-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), Physiologie de l'Insecte : Signalisation et Communication (PISC), Institut National de la Recherche Agronomique (INRA)-Université Pierre et Marie Curie - Paris 6 (UPMC)-AgroParisTech, Laboratoire Evolution, Génomes et Spéciation (LEGS), Centre National de la Recherche Scientifique (CNRS), Evolution, adaptation et comportement, Département écologie évolutive [LBBE], Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT), Laboratoire Navier (navier umr 8205), Institut Français des Sciences et Technologies des Transports, de l'Aménagement et des Réseaux (IFSTTAR)-École des Ponts ParisTech (ENPC)-Centre National de la Recherche Scientifique (CNRS), Évolution, génomes, comportement et écologie (EGCE), Université Paris-Sud - Paris 11 (UP11)-IRD-Centre National de la Recherche Scientifique (CNRS), GESTION DES DONNÉES ET DE LA CONNAISSANCE (IRISA-D7), Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Université de Bretagne Sud (UBS)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-Télécom Bretagne-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-CentraleSupélec-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Université de Rennes (UNIV-RENNES)-CentraleSupélec-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Université de Rennes (UNIV-RENNES)-CentraleSupélec-Inria Rennes – Bretagne Atlantique, Institut National de Recherche en Informatique et en Automatique (Inria), AGROCAMPUS OUEST-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National de la Recherche Agronomique (INRA), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Rennes 1 (UR1), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Université de Bretagne Sud (UBS)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National de Recherche en Informatique et en Automatique (Inria)-École normale supérieure - Rennes (ENS Rennes)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-CentraleSupélec-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Bretagne Sud (UBS)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-École normale supérieure - Rennes (ENS Rennes)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), and Centre National de la Recherche Scientifique (CNRS)-IRD-Université Paris-Sud - Paris 11 (UP11)

Subjects
next-generation se-quencing, Sesamia nonagrioides, Genes, Insect, Moths, Applied Microbiology and Biotechnology, Pheromones, Transcriptome, 0302 clinical medicine, Stemborer, Phylogeny, Genetics, Likelihood Functions, 0303 health sciences, biology, Reverse Transcriptase Polymerase Chain Reaction, High-Throughput Nucleotide Sequencing, [SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], Receptors, Pheromone, Smell, Sex pheromone, Pheromone, chemosensory receptors, Research Paper, pheromone biosynthesis, transcriptome, next-generation sequencing, Molecular Sequence Data, Zea mays, DNA sequencing, 03 medical and health sciences, Phylogenetics, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], Animals, Amino Acid Sequence, phéromone, Molecular Biology, Ecology, Evolution, Behavior and Systematics, DNA Primers, 030304 developmental biology, Base Sequence, Models, Genetic, Gene Expression Profiling, Computational Biology, Cell Biology, biology.organism_classification, Gene expression profiling, [INFO.INFO-BI]Computer Science [cs]/Bioinformatics [q-bio.QM], 030217 neurology & neurosurgery, Developmental Biology
Abstract

International audience; The stemborer Sesamia nonagrioides is an important pest of maize in the Mediterranean Basin. Like other moths, this noctuid uses its chemosensory system to efficiently interact with its environment. However, very little is known on the molecular mechanisms that underlie chemosensation in this species. Here, we used next-generation sequencing (454 and Illumina) on different tissues from adult and larvae, including chemosensory organs and female ovipositors, to describe the chemosensory transcriptome of S. nonagrioides and identify key molecular components of the pheromone production and detection systems. We identified a total of 68 candidate chemosen-sory genes in this species, including 31 candidate binding-proteins and 23 chemosensory receptors. In particular, we retrieved the three co-receptors Orco, IR25a and IR8a necessary for chemosensory receptor functioning. Focusing on the pheromonal communication system, we identified a new pheromone-binding protein in this species, four candidate pheromone receptors and 12 carboxylesterases as candidate acetate degrading enzymes. In addition, we identified enzymes putatively involved in S. nonagrioides pheromone biosynthesis, including a ∆11-desaturase and different acetyltransferases and reductases. RNAseq analyses and RT-PCR were combined to profile gene expression in different tissues. This study constitutes the first large scale description of chemosensory genes in S. nonagrioides.

Published
2013
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9. The use of the sex pheromone as an evolutionary solution to food source selection in caterpillars

Author

Didier Rochat, Emmanuelle Jacquin-Joly, Frédéric Marion-Poll, Nicolas Glaser, Kacem Rharrabe, Michel Renou, Christelle Monsempes, Erwan Poivet, Physiologie de l'Insecte, Signalisation et Communication [Versailles] (PISC), and Institut National de la Recherche Agronomique (INRA)

Subjects
Arthropod Antennae, Male, 0106 biological sciences, animal structures, [SDV]Life Sciences [q-bio], General Physics and Astronomy, Zoology, Spodoptera, 01 natural sciences, General Biochemistry, Genetics and Molecular Biology, Food Preferences, 03 medical and health sciences, pheromone, Botany, Animals, sex, Sensilla, Sex Attractants, Spodoptera littoralis, Caterpillar, 030304 developmental biology, 0303 health sciences, Larva, Multidisciplinary, biology, fungi, General Chemistry, caterpillars, biology.organism_classification, Biological Evolution, 010602 entomology, Sex pheromone, Insect Proteins, Pheromone, Female, sense organs
Abstract

Sex pheromones are released by adults of a species to elicit a sexual interaction with the other sex of the same species. Here we report an unexpected effect of a moth sex pheromone on the caterpillars of the same species. We demonstrate that larvae of the cotton leafworm Spodoptera littoralis are attracted by the moth sex pheromone and that this phenomenon is independent of sex determination. In addition, we show that the olfactory sensilla carried by the caterpillar antennae are sensitive to the pheromone and that the caterpillar sensilla express pheromone-binding proteins that are used by adult antennae to bind pheromone components. Finally, we demonstrate that the larvae are preferentially attracted to a food source when it contains the sex pheromone main component. A possible interpretation of these results is that the sex pheromone is used to promote food search in caterpillars, opening potential new routes for insect pest management.

Published
2012
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10. Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations

Author

Salim Bourras, A. Stachowiak, Bénédicte Ollivier, Hadi Quesneville, Juliette Linglin, Joelle Amselem, Laurent Duret, Marie-Hélène Balesdent, Conrad L. Schoch, Barbara J. Howlett, Véronique Anthouard, Pascal Bally, Gert H. J. Kema, Nicolas Glaser, Angela P. Van de Wouw, James K. Hane, Patrick Wincker, Jean Weissenbach, Azita Dilmaghani, Nicolas Lapalu, Arnaud Couloux, Lilian Gout, Jonathan Grandaubert, Richard P. Oliver, Michel Meyer, Lynda M. Ciuffetti, Isabelle Fudal, Joseph W. Spatafora, Claire Hoede, Victoria Dominguez, Julie Poulain, Kim May, Anton Cozijnsen, B. Gillian Turgeon, Stephen B. Goodwin, Alexandre Degrave, Adeline Simon, Christopher B. Lawrence, Thierry Rouxel, Brett M. Tyler, Delphine Vincent, BIOlogie et GEstion des Risques en agriculture (BIOGER), AgroParisTech-Institut National de la Recherche Agronomique (INRA), Unité de Recherche Génomique Info (URGI), 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), Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Bioinformatique, phylogénie et génomique évolutive (BPGE), Département PEGASE [LBBE] (PEGASE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Biodiversité, Gènes & Communautés (BioGeCo), Université de Bordeaux (UB)-Institut National de la Recherche Agronomique (INRA), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, 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)-Université Paris-Saclay, Institut National de la Recherche Agronomique (INRA)-Université de Bordeaux (UB), Rouxel, Thierry, Grandaubert, Jonathan, Marc-Henri Lebrun (INRA-Bioger), Francis Martin (INRA, Interactions arbres/micro-organismes, Champenoux, France), Genoscope, Institut de Genomique, CEA, France, Agence Nationale de la Recherche [ANR-07-GPLA-051G], ANR [ANR-06-BLAN-0399, ANR-07-GPLA-015], Australian Grains Research and Development Corporation, NIH, National Library of Medicine, U.S. National Science Foundation [DEB-0717476, IOS-0924861], 'Dothideomycete' community, INRA-SPE department, and 'Leptosphaeria maculans' scientific and applied community

Subjects
0106 biological sciences, multidisciplinary science, champignon, General Physics and Astronomy, plant, champignon pathogène, 01 natural sciences, Genome, avirulence, gene-transfer, Leptosphaeria maculans, Phylogeny, [SDV.MP.MYC]Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, Genetics, Base Composition, 0303 health sciences, Multidisciplinary, Effector, Fungal genetics, DNA transposable elements, fungal, Genome, Fungal, transposable elements, Transposable element, [SDV.OT]Life Sciences [q-bio]/Other [q-bio.OT], oilseed rape, pathogen effectors, leptosphaeria maculans, molecular sequence data, Biology, stem canker, Article, General Biochemistry, Genetics and Molecular Biology, 03 medical and health sciences, Ascomycota, Molecular evolution, transcription factors, Point Mutation, élément transposable, Gene, 030304 developmental biology, Whole genome sequencing, Base Sequence, molecular evolution, Bioint Moleculair Phytopathology, Computational Biology, Genetic Variation, Molecular Sequence Annotation, brassica-napus, Sequence Analysis, DNA, General Chemistry, biology.organism_classification, fungi, 010606 plant biology & botany
Abstract

Fungi are of primary ecological, biotechnological and economic importance. Many fundamental biological processes that are shared by animals and fungi are studied in fungi due to their experimental tractability. Many fungi are pathogens or mutualists and are model systems to analyse effector genes and their mechanisms of diversification. In this study, we report the genome sequence of the phytopathogenic ascomycete Leptosphaeria maculans and characterize its repertoire of protein effectors. The L. maculans genome has an unusual bipartite structure with alternating distinct guanine and cytosine-equilibrated and adenine and thymine (AT)-rich blocks of homogenous nucleotide composition. The AT-rich blocks comprise one-third of the genome and contain effector genes and families of transposable elements, both of which are affected by repeat-induced point mutation, a fungal-specific genome defence mechanism. This genomic environment for effectors promotes rapid sequence diversification and underpins the evolutionary potential of the fungus to adapt rapidly to novel host-derived constraints., Leptosphaeria maculans is a plant pathogen that causes stem canker of oilseed rape. Rouxel et al. sequence and describe the key features of the L. maculans genome, including partitioning into AT-rich blocks that are enriched in effector genes and transposable elements affected by repeat-induced point mutation.

Published
2011
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11. Epigenetic Control of Effector Gene Expression in the Plant Pathogenic Fungus Leptosphaeria maculans

Author

Mennat El Ghalid, Bénédicte Ollivier, Nicolas Glaser, Jessica L Soyer, Juliette Linglin, Marie-Hélène Balesdent, Lanelle R. Connolly, Isabelle Fudal, Michael Freitag, Thierry Rouxel, Jonathan Grandaubert, 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), and AgroParisTech-Institut National de la Recherche Agronomique (INRA)

Subjects
[SDV.SA]Life Sciences [q-bio]/Agricultural sciences, Cancer Research, gene-poor AT-isochores, Pathogenesis, Plant Science, Epigenesis, Genetic, Transcriptomes, Histones, RNA interference, Gene Expression Regulation, Fungal, Heterochromatin, Heterochromatin assembly, Axenic, Genetics (clinical), Genetics, biology, Effector, Agriculture, Genomics, Chromatin, Functional Genomics, Host-Pathogen Interaction, Epigenetics, Research Article, lcsh:QH426-470, Plant Pathogens, Mycology, Methylation, Microbiology, Ascomycota, Genome Analysis Tools, Microbial Control, Biology, Microbial Pathogens, Molecular Biology, Gene, Ecology, Evolution, Behavior and Systematics, Plant Diseases, Leptosphaeria maculans, Brassica napus, Fungi, SSPs, gene-rich GC-isochores, Histone-Lysine N-Methyltransferase, Plant Pathology, biology.organism_classification, lcsh:Genetics, Heterochromatin protein 1, Genome Expression Analysis
Abstract

Plant pathogens secrete an arsenal of small secreted proteins (SSPs) acting as effectors that modulate host immunity to facilitate infection. SSP-encoding genes are often located in particular genomic environments and show waves of concerted expression at diverse stages of plant infection. To date, little is known about the regulation of their expression. The genome of the Ascomycete Leptosphaeria maculans comprises alternating gene-rich GC-isochores and gene-poor AT-isochores. The AT-isochores harbor mosaics of transposable elements, encompassing one-third of the genome, and are enriched in putative effector genes that present similar expression patterns, namely no expression or low-level expression during axenic cultures compared to strong induction of expression during primary infection of oilseed rape (Brassica napus). Here, we investigated the involvement of one specific histone modification, histone H3 lysine 9 methylation (H3K9me3), in epigenetic regulation of concerted effector gene expression in L. maculans. For this purpose, we silenced the expression of two key players in heterochromatin assembly and maintenance, HP1 and DIM-5 by RNAi. By using HP1-GFP as a heterochromatin marker, we observed that almost no chromatin condensation is visible in strains in which LmDIM5 was silenced by RNAi. By whole genome oligoarrays we observed overexpression of 369 or 390 genes, respectively, in the silenced-LmHP1 and -LmDIM5 transformants during growth in axenic culture, clearly favouring expression of SSP-encoding genes within AT-isochores. The ectopic integration of four effector genes in GC-isochores led to their overexpression during growth in axenic culture. These data strongly suggest that epigenetic control, mediated by HP1 and DIM-5, represses the expression of at least part of the effector genes located in AT-isochores during growth in axenic culture. Our hypothesis is that changes of lifestyle and a switch toward pathogenesis lift chromatin-mediated repression, allowing a rapid response to new environmental conditions., Author Summary Effectors are key players in pathogenicity of microbes toward plants. Effector genes usually show concerted expression during plant infection but how this concerted expression is generated remains a largely unexplored research topic. Epigenetic mechanisms are involved in genome maintenance and integrity but are increasingly considered as important for regulation of gene expression in numerous and diverse organisms. Here we show that the genomic environment has impact on expression of Leptosphaeria maculans effector genes, and that an epigenetic mechanism that relies on two proteins involved in heterochromatin formation and maintenance, HP1 and DIM-5, modulates this expression, leading to repression during growth in axenic culture. Chromatin decondensation by removal of histone H3 lysine 9 methylation and/or HP1 is presumably a prerequisite for effector gene expression during primary infection of oilseed rape. Thus we show chromatin-based transcriptional regulation that can act on effector gene expression in fungi. Our study highlights the importance of heterochromatic landscapes, not only for genome maintenance but also in rapid and efficient adaptation of organisms to changing environmental situations.

Published
2014
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