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1. Quantitative resistance to clubroot infection mediated by transgenerational epigenetic variation in Arabidopsis

Author

Benjamin Liegard, Mathilde Etcheverry, Mélanie Jubault, Victoire Baillet, Christine Lariagon, Evens Joseph, Maria J. Manzanares-Dauleux, Antoine Gravot, Aurélie Evrard, Vincent Colot, Jocelyne Lemoine, 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 de biologie de l'ENS Paris (UMR 8197/1024) (IBENS), Département de Biologie - ENS Paris, École normale supérieure - Paris (ENS Paris), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS Paris), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), This research was supported by AGROCAMPUS OUEST, INRA and Université de Rennes. Benjamin Liégard was a PhD student co-funded by INRA BAP department and Brittany Region., Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Institut de biologie de l'ENS Paris (IBENS), École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS-PSL), Colot, Vincent, AGROCAMPUS OUEST-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National de la Recherche Agronomique (INRA), École normale supérieure - Paris (ENS Paris)-École normale supérieure - Paris (ENS Paris)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Département de Biologie - ENS Paris, and Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)

Subjects
0106 biological sciences, 0301 basic medicine, Physiology, Inheritance Patterns, Arabidopsis, Plant Science, methylome, Plasmodiophorida, [SDV.BBM.BM] Life Sciences [q-bio]/Biochemistry, Molecular Biology/Molecular biology, 01 natural sciences, Epigenesis, Genetic, [SDV.GEN.GPL] Life Sciences [q-bio]/Genetics/Plants genetics, [SDV.BV] Life Sciences [q-bio]/Vegetal Biology, Disease Resistance, Genetics, [SDV.BIBS] Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], Full Paper, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], Temperature, food and beverages, Full Papers, [SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], Phenotype, Plasmodiophora brassicae, DNA methylation, [SDV.BBM.GTP] Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], quantitative resistance, Quantitative Trait Loci, clubroot, Biology, Plant disease resistance, Quantitative trait locus, Clubroot, [SDV.GEN.GPL]Life Sciences [q-bio]/Genetics/Plants genetics, 03 medical and health sciences, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], medicine, [SDV.BID.EVO] Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, transgenerational, Epigenetics, Allele, Gene, Plant Diseases, [SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE], Base Sequence, epigenetics, Research, Genetic Variation, epigenet- ics, [SDV.BBM.BM]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Molecular biology, DNA Methylation, medicine.disease, biology.organism_classification, EpiRIL, 030104 developmental biology, Mutation, [SDV.GEN.GPO] Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE], 010606 plant biology & botany
Abstract

International audience; Quantitative disease resistance, often influenced by environmental factors, is thought to be the result of DNA sequence variants segregating at multiple loci. However, heritable differences in DNA methylation, so-called transgenerational epigenetic variants, also could contribute to quantitative traits. Here, we tested this possibility using the well-characterized quantitative resistance of Arabidopsis to clubroot, a Brassica major disease caused by Plasmodiophora brassicae. For that, we used the epigenetic recombinant inbred lines (epiRIL) derived from the cross ddm1-2 9 Col-0, which show extensive epigenetic variation but limited DNA sequence variation. Quantitative loci under epigenetic control (QTL epi) mapping was carried out on 123 epiRIL infected with P. brassicae and using various disease-related traits. EpiRIL displayed a wide range of continuous phenotypic responses. Twenty QTL epi were detected across the five chromosomes, with a bona fide epigenetic origin for 16 of them. The effect of five QTL epi was dependent on temperature conditions. Six QTL epi co-localized with previously identified clubroot resistance genes and QTL in Arabidopsis. Co-localization of clubroot resistance QTL epi with previously detected DNA-based QTL reveals a complex model in which a combination of allelic and epiallelic variations interacts with the environment to lead to variation in clubroot quantitative resistance.

Published
2019
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2. Identification and characterisation of hypomethylated DNA loci controlling quantitative resistance in Arabidopsis

Author

Ritushree Jain, Jurriaan Ton, Frank Johannes, Vincent Colot, Leonardo Furci, Victoire Baillet, Joost H. M. Stassen, James Whelan, David Roquis, Oliver Berkowitz, La Trobe University, La Trobe University [Melbourne], Ecologie et évolution des interactions [2011-2014] (2EI), Université de Perpignan Via Domitia (UPVD)-Centre National de la Recherche Scientifique (CNRS), Institut de biologie de l'ENS Paris (IBENS), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Département de Biologie - ENS Paris, École normale supérieure - Paris (ENS Paris), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS Paris), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Department of Animal and Plant Sciences [Sheffield], University of Sheffield [Sheffield], Institut de biologie de l'ENS Paris (UMR 8197/1024) (IBENS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Département de Biologie - ENS Paris, Unité de recherche en génomique végétale (URGV), Institut National de la Recherche Agronomique (INRA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Ecologie et évolution des interactions (2EI), Département de Biologie - ENS Paris, École normale supérieure - Paris (ENS Paris)-École normale supérieure - Paris (ENS Paris)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Université d'Évry-Val-d'Essonne (UEVE)-Institut National de la Recherche Agronomique (INRA), Centre National de la Recherche Scientifique (CNRS)-Université de Perpignan Via Domitia (UPVD), and Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Epigenomics, 0106 biological sciences, 0301 basic medicine, plant immune signalling, Arabidopsis, Plant Biology, 01 natural sciences, Epigenesis, Genetic, Transcriptome, Gene Expression Regulation, Plant, Cluster Analysis, Biology (General), ComputingMilieux_MISCELLANEOUS, Disease Resistance, 2. Zero hunger, Genetics, education.field_of_study, biology, General Neuroscience, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], General Medicine, [SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], ddc, Phenotype, Oomycetes, DNA methylation, Medicine, Research Article, DNA, Plant, QH301-705.5, Science, Centromere, Quantitative Trait Loci, Population, plant-microbe interactions, Quantitative trait locus, Genes, Plant, General Biochemistry, Genetics and Molecular Biology, DNA sequencing, [SDV.GEN.GPL]Life Sciences [q-bio]/Genetics/Plants genetics, 03 medical and health sciences, Quantitative Trait, Heritable, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, Epigenetics, education, Gene, Plant Diseases, Hyaloperonospora arabidopsidis, [SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE], General Immunology and Microbiology, Sequence Analysis, RNA, Gene Expression Profiling, [SDV.BBM.BM]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Molecular biology, DNA Methylation, biology.organism_classification, 030104 developmental biology, Haplotypes, A. thaliana, 010606 plant biology & botany
Abstract

Variation in DNA methylation enables plants to inherit traits independently of changes to DNA sequence. Here, we have screened an Arabidopsis population of epigenetic recombinant inbred lines (epiRILs) for resistance against Hyaloperonospora arabidopsidis (Hpa). These lines share the same genetic background, but show variation in heritable patterns of DNA methylation. We identified four epigenetic quantitative trait loci (epiQTLs) that provide quantitative resistance without reducing plant growth or resistance to other (a)biotic stresses. Phenotypic characterisation and RNA-sequencing analysis revealed that Hpa-resistant epiRILs are primed to activate defence responses at the relatively early stages of infection. Collectively, our results show that hypomethylation at selected pericentromeric regions is sufficient to provide quantitative disease resistance, which is associated with genome-wide priming of defence-related genes. Based on comparisons of global gene expression and DNA methylation between the wild-type and resistant epiRILs, we discuss mechanisms by which the pericentromeric epiQTLs could regulate the defence-related transcriptome., eLife digest In plants, animals and microbes genetic information is encoded by DNA, which are made up of sequences of building blocks, called nucleotide bases. These sequences can be separated into sections known as genes that each encode specific traits. It was previously thought that only changes to the sequence of bases in a DNA molecule could alter the traits passed on to future generations. However, it has recently become clear that some traits can also be inherited through modifications to the DNA that do not alter its sequence. One such modification is to attach a tag, known as a methyl group, to a nucleotide base known as cytosine. These methyl tags can be added to, or removed from, DNA to create different patterns of methylation. Previous studies have shown that plants whose DNA is less methylated than normal (‘hypo-methylated’) are more resistant to plant diseases. However, the location and identity of the hypo-methylated DNA regions controlling this resistance remained unknown. To address this problem, Furci, Jain et al. studied how DNA methylation in a small weed known as Arabidopsis thaliana affects how well the plants can resist a disease known as downy mildew. Furci, Jain et al. studied a population of over 100 A. thaliana lines that have the same DNA sequences but different patterns of DNA methylation. The experiments identified four DNA locations that were less methylated in lines with enhanced resistance to downy mildew. Importantly, this form of resistance did not appear to reduce how well the plants grew, or make them less able to resist other diseases or environmental stresses. The results of further experiments suggested that reduced methylation at the four DNA regions prime the plant’s immune system, enabling a faster and stronger activation of a multitude of defence genes across the genome after attack by downy mildew. The next steps following on from this work are to investigate exactly how the four DNA regions with reduced methylation can prime so many different defence genes in the plant. Further research is also needed to determine whether it is possible to breed crop plants with lower levels of methylation at specific DNA locations to improve disease resistance, but without decreasing the amount and quality of food produced.

Published
2019
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