DNA hypomethylation of the host tree impairs interaction with mutualistic ectomycorrhizal fungus.
DEMETER
DNA METHYLATION 1
DNA demethylatione
Laccaria bicolor
mycorrhizas
pigenetic
poplar
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
received:
22
07
2022
accepted:
21
12
2022
medline:
19
5
2023
pubmed:
23
2
2023
entrez:
22
2
2023
Statut:
ppublish
Résumé
Ectomycorrhizas are an intrinsic component of tree nutrition and responses to environmental variations. How epigenetic mechanisms might regulate these mutualistic interactions is unknown. By manipulating the level of expression of the chromatin remodeler DECREASE IN DNA METHYLATION 1 (DDM1) and two demethylases DEMETER-LIKE (DML) in Populus tremula × Populus alba lines, we examined how host DNA methylation modulates multiple parameters of the responses to root colonization with the mutualistic fungus Laccaria bicolor. We compared the ectomycorrhizas formed between transgenic and wild-type (WT) trees and analyzed their methylomes and transcriptomes. The poplar lines displaying lower mycorrhiza formation rate corresponded to hypomethylated overexpressing DML or RNAi-ddm1 lines. We found 86 genes and 288 transposable elements (TEs) differentially methylated between WT and hypomethylated lines (common to both OX-dml and RNAi-ddm1) and 120 genes/1441 TEs in the fungal genome suggesting a host-induced remodeling of the fungal methylome. Hypomethylated poplar lines displayed 205 differentially expressed genes (cis and trans effects) in common with 17 being differentially methylated (cis). Our findings suggest a central role of host and fungal DNA methylation in the ability to form ectomycorrhizas including not only poplar genes involved in root initiation, ethylene and jasmonate-mediated pathways, and immune response but also terpenoid metabolism.
Substances chimiques
DNA
9007-49-2
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2561-2577Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2023 The Authors New Phytologist © 2023 New Phytologist Foundation This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.
Références
Abdulsalam O, Wagner K, Wirth S, Kunert M, David A, Kallenbach M, Boland W, Kothe E, Krause K. 2021. Phytohormones and volatile organic compounds, like geosmin, in the ectomycorrhiza of Tricholoma vaccinum and Norway spruce (Picea abies). Mycorrhiza 31: 173-188.
Akalin A, Kormaksson M, Li S, Garrett-Bakelman FE, Figueroa ME, Melnick A, Mason CE. 2012. methylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biology 13: R87.
Alonso C, Ramos-Cruz D, Becker C. 2018. The role of plant epigenetics in biotic interactions. New Phytologist 221: 731-737.
Balestrini R, Kottke I. 2016. Structure and development of ectomycorrhizal roots. In: Martin F, ed. Molecular mycorrhizal symbiosis. Hoboken, NJ, USA: John Wiley & Sons, 47-61.
Basso V, Kohler A, Miyauchi S, Singan V, Guinet F, Šimura J, Novák O, Barry KW, Amirebrahimi M, Block J et al. 2020. An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots. Plant, Cell & Environment 43: 1047-1068.
Bewick AJ, Hofmeister BT, Powers RA, Mondo SJ, Grigoriev IV, James TY, Stajich JE, Schmitz RJ. 2019. Diversity of cytosine methylation across the fungal tree of life. Nature Ecology & Evolution 3: 479-490.
Bouffaud M-L, Herrmann S, Tarkka MT, Bönn M, Feldhahn L, Buscot F. 2020. Oak displays common local but specific distant gene regulation responses to different mycorrhizal fungi. BMC Genomics 21: 399.
Conde D, Le Gac A, Perales M, Dervinis C, Kirst M, Maury S, González-Melendi P, Allona I. 2017a. Chilling-responsive DEMETER-LIKE DNA demethylase mediates in poplar bud break. Plant, Cell & Environment 40: 2236-2249.
Conde D, Moreno-Cortés A, Dervinis C, Ramos-Sánchez JM, Kirst M, Perales M, González-Melendi P, Allona I. 2017b. Overexpression of DEMETER, a DNA demethylase, promotes early apical bud maturation in poplar. Plant, Cell & Environment 40: 2806-2819.
Conde D, Perales M, Sreedasyam A, Tuskan GA, Lloret A, Badenes ML, González-Melendi P, Ríos G, Allona I. 2019. Engineering tree seasonal cycles of growth through chromatin modification. Frontiers in Plant Science 10: 412.
Corbin KR, Bolt B, Rodríguez López CM. 2020. Breeding for beneficial microbial communities using epigenomics. Frontiers in Microbiology 11: 937.
Couto D, Zipfel C. 2016. Regulation of pattern recognition receptor signalling in plants. Nature Reviews. Immunology 16: 537-552.
Danchin E. 2013. Avatars of information: towards an inclusive evolutionary synthesis. Trends in Ecology & Evolution 28: 351-358.
Ditengou FA, Müller A, Rosenkranz M, Felten J, Lasok H, van Doorn MM, Legué V, Palme K, Schnitzler J-P, Polle A. 2015. Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogramms root architecture. Nature Communications 6: 62-79.
Doyle JJ, Doyle JL, eds. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11-15.
Dreischhoff S, Das IS, Jakobi M, Kasper K, Polle A. 2020. Local responses and systemic induced resistance mediated by ectomycorrhizal fungi. Frontiers in Plant Science 11: 590063.
Dugé de Bernonville T, Daviaud C, Chaparro C, Tost J, Maury S. 2022. From methylome to integrative analysis of tissue specificity. Methods in Molecular Biology 2505: 223-240.
Erdmann RM, Picard CL. 2020. RNA-directed DNA methylation. PLoS Genetics 16: e1009034.
Felten J, Kohler A, Morin E, Bhalerao RP, Palme K, Martin F, Ditengou FA, Legué V. 2009. The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiology 151: 1991-2005.
Feng S, Cokus SJ, Zhang X, Chen P-Y, Bostick M, Goll MG, Hetzel J, Jain J, Strauss SH, Halpern ME et al. 2010. Conservation and divergence of methylation patterning in plants and animals. Proceedings of the National Academy of Sciences, USA 107: 8689-8694.
Fracchia F, Mangeot-Peter L, Jacquot L, Martin F, Veneault-Fourrey C, Deveau A. 2021. Colonization of naive roots from Populus tremula × alba involves successive waves of fungi and bacteria with different trophic abilities. Applied and Environmental Microbiology 87: e02541-20.
Ghoshal B, Picard CL, Vong B, Feng S, Jacobsen SE. 2021. CRISPR-based targeting of DNA methylation in Arabidopsis thaliana by a bacterial CG-specific DNA methyltransferase. Proceedings of the National Academy of Sciences, USA 118: e2125016118.
Gourcilleau D, Lenne C, Armenise C, Moulia B, Julien J-L, Bronner G, Leblanc-Fournier N. 2011. Phylogenetic study of plant Q-type C2H2 zinc finger proteins and expression analysis of poplar genes in response to osmotic, cold and mechanical stresses. DNA Research 18: 77-92.
Halter T, Wang J, Amesefe D, Lastrucci E, Charvin M, Singla Rastogi M, Navarro L. 2021. The Arabidopsis active demethylase ROS1 cis-regulates defence genes by erasing DNA methylation at promoter-regulatory regions. eLife 10: e62994.
Hannan Parker A, Wilkinson SW, Ton J. 2022. Epigenetics: a catalyst of plant immunity against pathogens. New Phytologist 233: 66-83.
He C, Zhang Z, Li B, Tian S. 2020. The pattern and function of DNA methylation in fungal plant pathogens. Microorganisms 8: 227.
van der Heijden MGA, Martin FM, Selosse M-A, Sanders IR. 2015. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytologist 205: 1406-1423.
Huang C-Y, Jin H. 2022. Coordinated epigenetic regulation in plants: a potent managerial tool to conquer biotic stress. Frontiers in Plant Science 12: 795274.
Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski A, Albuisson J, Heredia F, Audigier P et al. 2009. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genetics 5: e1000530.
Kakoulidou I, Avramidou EV, Baránek M, Brunel-Muguet S, Farrona S, Johannes F, Kaiserli E, Lieberman-Lazarovich M, Martinelli F, Mladenov V et al. 2021. Epigenetics for crop improvement in times of global change. Biology 10: 766.
Kaling M, Schmidt A, Moritz F, Rosenkranz M, Witting M, Kasper K, Janz D, Schmitt-Kopplin P, Schnitzler J-P, Polle A. 2018. Mycorrhiza-triggered transcriptomic and metabolomic networks impinge on herbivore fitness. Plant Physiology 176: 2639-2656.
Kang H, Chen X, Kemppainen M, Pardo AG, Veneault-Fourrey C, Kohler A, Martin FM. 2020. The small secreted effector protein MiSSP7.6 of Laccaria bicolor is required for the establishment of ectomycorrhizal symbiosis. Environmental Microbiology 22: 1435-1446.
Kottke I, Oberwinkler F. 1990. Comparative investigations on the differentiation of the endodermis and the development of the Hartig net in mycorrhizae of Picea abies and Larix decidua. Trees 4: 41-48.
Labbé J, Muchero W, Czarnecki O, Wang J, Wang X, Bryan AC, Zheng K, Yang Y, Xie M, Zhang J et al. 2019. Mediation of plant-mycorrhizal interaction by a lectin receptor-like kinase. Nature Plants 5: 676-680.
Lafon-Placette C, Faivre-Rampant P, Delaunay A, Street N, Brignolas F, Maury S. 2013. Methylome of DNase I sensitive chromatin in Populus trichocarpa shoot apical meristematic cells: a simplified approach revealing characteristics of gene-body DNA methylation in open chromatin state. New Phytologist 197: 416-430.
Lafon-Placette C, Le Gac A-L, Chauveau D, Segura V, Delaunay A, Lesage-Descauses M-C, Hummel I, Cohen D, Jesson B, Le Thiec D et al. 2018. Changes in the epigenome and transcriptome of the poplar shoot apical meristem in response to water availability affect preferentially hormone pathways. Journal of Experimental Botany 69: 537-551.
Lanciano S, Carpentier M-C, Llauro C, Jobet E, Robakowska-Hyzorek D, Lasserre E, Ghesquière A, Panaud O, Mirouze M. 2017. Sequencing the extrachromosomal circular mobilome reveals retrotransposon activity in plants. PLoS Genetics 13: e1006630.
Le Gac A-L, Lafon-Placette C, Chauveau D, Segura V, Delaunay A, Fichot R, Marron N, Le Jan I, Berthelot A, Bodineau G et al. 2018. Winter-dormant shoot apical meristem in poplar trees shows environmental epigenetic memory. Journal of Experimental Botany 69: 4821-4837.
Lehto T, Zwiazek JJ. 2011. Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21: 71-90.
Lloyd JPB, Lister R. 2022. Epigenome plasticity in plants. Nature Reviews. Genetics 23: 55-68.
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15: 550.
Luo C, Hajkova P, Ecker JR. 2018. Dynamic DNA methylation: in the right place at the right time. Science 361: 1336-1340.
Maher B. 2008. Personal genomes: the case of the missing heritability. Nature News 456: 18-21.
Marqués-Gálvez JE, Veneault-Fourrey C, Kohler A. 2022. Ectomycorrhizal symbiosis: from genomics to trans-kingdom molecular communication and signaling. In: Hortwitz BA, Mukherjee PK, eds. Microbial cross-talk in the rhizosphere, rhizosphere biology. Singapore City, Singapore: Springer, 273-296.
Martin F, Kohler A, Murat C, Veneault-Fourrey C, Hibbett DS. 2016. Unearthing the roots of ectomycorrhizal symbioses. Nature Reviews. Microbiology 14: 760-773.
Maury S, Sow MD, Le Gac A-L, Genitoni J, Lafon-Placette C, Mozgova I. 2019. Phytohormone and chromatin crosstalk: the missing link for developmental plasticity? Frontiers in Plant Science 10: 395.
Meyer P. 2015. Epigenetic variation and environmental change. Journal of Experimental Botany 66: 3541-3548.
Mhiri C, Borges F, Grandbastien M-A. 2022. Specificities and dynamics of transposable elements in land plants. Biology 11: 488.
Miyauchi S, Kiss E, Kuo A, Drula E, Kohler A, Sánchez-García M, Morin E, Andreopoulos B, Barry KW, Bonito G et al. 2020. Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. Nature Communications 11: 5125.
Monteiro F, Nishimura MT. 2018. Structural, functional, and genomic diversity of plant NLR proteins: an evolved resource for rational engineering of plant immunity. Annual Review of Phytopathology 56: 243-267.
Muyle AM, Seymour DK, Lv Y, Huettel B, Gaut BS. 2022. Gene body methylation in plants: mechanisms, functions, and important implications for understanding evolutionary processes. Genome Biology and Evolution 14: evac038.
Nagymihály M, Veluchamy A, Györgypál Z, Ariel F, Jégu T, Benhamed M, Szűcs A, Kereszt A, Mergaert P, Kondorosi É. 2017. Ploidy-dependent changes in the epigenome of symbiotic cells correlate with specific patterns of gene expression. Proceedings of the National Academy of Sciences, USA 114: 4543-4548.
Niederhuth CE, Bewick AJ, Ji L, Alabady MS, Kim KD, Li Q, Rohr NA, Rambani A, Burke JM, Udall JA et al. 2016. Widespread natural variation of DNA methylation within angiosperms. Genome Biology 17: 194.
Niyikiza D, Piya S, Routray P, Miao L, Kim W-S, Burch-Smith T, Gill T, Sams C, Arelli PR, Pantalone V et al. 2020. Interactions of gene expression, alternative splicing, and DNA methylation in determining nodule identity. The Plant Journal 103: 1744-1766.
Pellegrin C, Daguerre Y, Ruytinx J, Guinet F, Kemppainen M, Frey NFD, Puech-Pagès V, Hecker A, Pardo AG, Martin FM et al. 2019. Laccaria bicolor MiSSP8 is a small-secreted protein decisive for the establishment of the ectomycorrhizal symbiosis. Environmental Microbiology 21: 3765-3779.
Péret B, De Rybel B, Casimiro I, Benková E, Swarup R, Laplaze L, Beeckman T, Bennett MJ. 2009. Arabidopsis lateral root development: an emerging story. Trends in Plant Science 14: 399-408.
Plett JM, Daguerre Y, Wittulsky S, Vayssières A, Deveau A, Melton SJ, Kohler A, Morrell-Falvey JL, Brun A, Veneault-Fourrey C et al. 2014a. Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes. Proceedings of the National Academy of Sciences, USA 111: 8299-8304.
Plett JM, Khachane A, Ouassou M, Sundberg B, Kohler A, Martin F. 2014b. Ethylene and jasmonic acid act as negative modulators during mutualistic symbiosis between Laccaria bicolor and Populus roots. New Phytologist 202: 270-286.
Plett JM, Kohler A, Khachane A, Keniry K, Plett KL, Martin F, Anderson IC. 2015. The effect of elevated carbon dioxide on the interaction between Eucalyptus grandis and diverse isolates of Pisolithus sp. is associated with a complex shift in the root transcriptome. New Phytologist 206: 1423-1436.
Plett KL, Raposo AE, Anderson IC, Piller SC, Plett JM. 2019. Protein arginine methyltransferase expression affects ectomycorrhizal symbiosis and the regulation of hormone signaling pathways. Molecular Plant-Microbe Interactions 32: 1291-1302.
Quesneville H. 2020. Twenty years of transposable element analysis in the Arabidopsis thaliana genome. Mobile DNA 11: 28.
Ramakrishnan M, Satish L, Kalendar R, Narayanan M, Kandasamy S, Sharma A, Emamverdian A, Wei Q, Zhou M. 2021. The dynamism of transposon methylation for plant development and stress adaptation. International Journal of Molecular Sciences 22: 11387.
Ramos-Cruz D, Troyee AN, Becker C. 2021. Epigenetics in plant organismic interactions. Current Opinion in Plant Biology 61: 102060.
Russo VEA, Riggs AD, Martienssen RA. 1996. Epigenetic mechanisms of gene regulation. Cold Spring Harbour, NY, USA: Cold Spring Harbour Laboratory Press.
Satgé C, Moreau S, Sallet E, Lefort G, Auriac M-C, Remblière C, Cottret L, Gallardo K, Noirot C, Jardinaud M-F et al. 2016. Reprogramming of DNA methylation is critical for nodule development in Medicago truncatula. Nature Plants 2: 16166.
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B et al. 2012. Fiji: an open-source platform for biological-image analysis. Nature Methods 9: 676-682.
Schmitz RJ, Lewis ZA, Goll MG. 2019. DNA methylation: shared and divergent features across eukaryotes. Trends in Genetics 35: 818-827.
Schweiger R, Müller C. 2015. Leaf metabolome in arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology 26: 120-126.
Sebastiana M, Gargallo-Garriga A, Sardans J, Pérez-Trujillo M, Monteiro F, Figueiredo A, Maia M, Nascimento R, Silva MS, Ferreira AN et al. 2021. Metabolomics and transcriptomics to decipher molecular mechanisms underlying ectomycorrhizal root colonization of an oak tree. Scientific Reports 11: 8576.
Sebastiana M, Vieira B, Lino-Neto T, Monteiro F, Figueiredo A, Sousa L, Pais MS, Tavares R, Paulo OS. 2014. Oak root response to ectomycorrhizal symbiosis establishment: RNA-Seq derived transcript identification and expression profiling. PLoS ONE 9: e98376.
Seymour DK, Becker C. 2017. The causes and consequences of DNA methylome variation in plants. Current Opinion in Plant Biology 36: 56-63.
Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. London, UK: Academic Press.
Sow MD, Le Gac A-L, Fichot R, Lanciano S, Delaunay A, Le Jan I, Lesage-Descauses M-C, Citerne S, Caius J, Brunaud V et al. 2021. RNAi suppression of DNA methylation affects the drought stress response and genome integrity in transgenic poplar. New Phytologist 232: 80-97.
Soyer JL, Rouxel T, Fudal I. 2015. Chromatin-based control of effector gene expression in plant-associated fungi. Current Opinion in Plant Biology 26: 51-56.
Su Y-H, Liu Y-B, Zhang X-S. 2011. Auxin-cytokinin interaction regulates meristem development. Molecular Plant 4: 616-625.
Tschaplinski TJ, Plett JM, Engle NL, Deveau A, Cushman KC, Martin MZ, Doktycz MJ, Tuskan GA, Brun A, Kohler A et al. 2014. Populus trichocarpa and Populus deltoides exhibit different metabolomic responses to colonization by the symbiotic fungus Laccaria bicolor. Molecular Plant-Microbe Interactions 27: 546-556.
Varga S, Soulsbury CD. 2017. Paternal arbuscular mycorrhizal fungal status affects DNA methylation in seeds. Biology Letters 13: 20170407.
Varga S, Soulsbury CD. 2019. Arbuscular mycorrhizal fungi change host plant DNA methylation systemically. Plant Biology 21: 278-283.
Vining KJ, Pomraning KR, Wilhelm LJ, Priest HD, Pellegrini M, Mockler TC, Freitag M, Strauss SH. 2012. Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression. BMC Genomics 13: 27.
Wasserstein RL, Lazar NA. 2016. The ASA statement on P-values: context, process, and purpose. The American Statistician 70: 129-133.
Williams BP, Bechen LL, Pohlmann DA, Gehring M. 2022. Somatic DNA demethylation generates tissue-specific methylation states and impacts flowering time. Plant Cell 34: 1189-1206.
Wong-Bajracharya J, Lutz A, Natera S, Wang M, Ng V, Grigoriev I, Martin F, Roessner U, Anderson I, Plett J. 2019. The influence of contrasting microbial lifestyles on the pre-symbiotic metabolite responses of Eucalyptus grandis roots. Frontiers in Ecology and Evolution 7: 10.
Yi F, Jia Z, Xiao Y, Ma W, Wang J. 2018. SPTEdb: a database for transposable elements in salicaceous plants. Database 2018: bay024.
Zhang F, Anasontzis GE, Labourel A, Champion C, Haon M, Kemppainen M, Commun C, Deveau A, Pardo A, Veneault-Fourrey C et al. 2018. The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development. New Phytologist 220: 1309-1321.
Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW-L, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE et al. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126: 1189-1201.
Zhou Y, Zhou B, Pache L, Chang M, Khodabakhshi AH, Tanaseichuk O, Benner C, Chanda SK. 2019. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nature Communications 10: 1523.
Zhu Q-H, Shan W-X, Ayliffe MA, Wang M-B. 2016. Epigenetic mechanisms: an emerging player in plant-microbe interactions. Molecular Plant-Microbe Interactions 29: 187-196.
Zhu R, Shevchenko O, Ma C, Maury S, Freitag M, Strauss SH. 2013. Poplars with a PtDDM1-RNAi transgene have reduced DNA methylation and show aberrant post-dormancy morphology. Planta 237: 1483-1493.