The plant NADPH oxidase RBOHD is required for microbiota homeostasis in leaves.


Journal

Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869

Informations de publication

Date de publication:
07 2021
Historique:
received: 10 01 2021
accepted: 25 05 2021
entrez: 1 7 2021
pubmed: 2 7 2021
medline: 21 9 2021
Statut: ppublish

Résumé

The plant microbiota consists of a multitude of microorganisms that can affect plant health and fitness. However, it is currently unclear how the plant shapes its leaf microbiota and what role the plant immune system plays in this process. Here, we evaluated Arabidopsis thaliana mutants with defects in different parts of the immune system for an altered bacterial community assembly using a gnotobiotic system. While higher-order mutants in receptors that recognize microbial features and in defence hormone signalling showed substantial microbial community alterations, the absence of the plant NADPH oxidase RBOHD caused the most pronounced change in the composition of the leaf microbiota. The rbohD knockout resulted in an enrichment of specific bacteria. Among these, we identified Xanthomonas strains as opportunistic pathogens that colonized wild-type plants asymptomatically but caused disease in rbohD knockout plants. Strain dropout experiments revealed that the lack of RBOHD unlocks the pathogenicity of individual microbiota members driving dysbiosis in rbohD knockout plants. For full protection, healthy plants require both a functional immune system and a microbial community. Our results show that the NADPH oxidase RBOHD is essential for microbiota homeostasis and emphasizes the importance of the plant immune system in controlling the leaf microbiota.

Identifiants

pubmed: 34194036
doi: 10.1038/s41564-021-00929-5
pii: 10.1038/s41564-021-00929-5
pmc: PMC7612668
mid: EMS126426
doi:

Substances chimiques

Arabidopsis Proteins 0
respiratory burst oxidase homolog D, Arabidopsis EC 1.6.-
NADPH Oxidases EC 1.6.3.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

852-864

Subventions

Organisme : European Research Council
ID : 668991
Pays : International

Références

Beattie, G. A. & Lindow, S. E. Bacterial colonization of leaves: a spectrum of strategies. Phytopathol. 89, 353–359 (1999).
doi: 10.1094/PHYTO.1999.89.5.353
Vorholt, J. A. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10, 828–840 (2012).
pubmed: 23154261 doi: 10.1038/nrmicro2910
Pieterse, C. M. et al. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52, 347–375 (2014).
pubmed: 24906124 doi: 10.1146/annurev-phyto-082712-102340
Müller, D. B., Vogel, C., Bai, Y. & Vorholt, J. A. The plant microbiota: systems-level insights and perspectives. Annu. Rev. Genet. 50, 211–234 (2016).
pubmed: 27648643 doi: 10.1146/annurev-genet-120215-034952
Lugtenberg, B. & Kamilova, F. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541–556 (2009).
pubmed: 19575558 doi: 10.1146/annurev.micro.62.081307.162918
Berens, M. L., Berry, H. M., Mine, A., Argueso, C. T. & Tsuda, K. Evolution of hormone signaling networks in plant defense. Annu. Rev. Phytopathol. 55, 401–425 (2017).
pubmed: 28645231 doi: 10.1146/annurev-phyto-080516-035544
Cook, D. E., Mesarich, C. H. & Thomma, B. P. H. J. Understanding plant immunity as a surveillance system to detect invasion. Annu. Rev. Phytopathol. 53, 541–563 (2015).
pubmed: 26047564 doi: 10.1146/annurev-phyto-080614-120114
Teixeira, P. J. P. L., Colaianni, N. R., Fitzpatrick, C. R. & Dangl, J. L. Beyond pathogens: microbiota interactions with the plant immune system. Curr. Opin. Microbiol. 49, 7–17 (2019).
pubmed: 31563068 doi: 10.1016/j.mib.2019.08.003
Yu, K., Pieterse, C. M. J., Bakker, P. A. H. M. & Berendsen, R. L. Beneficial microbes going underground of root immunity. Plant Cell Environ. 42, 2860–2870 (2019).
pubmed: 31353481 pmcid: 6851990 doi: 10.1111/pce.13632
Hacquard, S., Spaepen, S., Garrido-Oter, R. & Schulze-Lefert, P. Interplay between innate immunity and the plant microbiota. Annu. Rev. Phytopathol. 55, 565–589 (2017).
pubmed: 28645232 doi: 10.1146/annurev-phyto-080516-035623
Lebeis, S. L. et al. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349, 860–864 (2015).
pubmed: 26184915 doi: 10.1126/science.aaa8764
Castrillo, G. et al. Root microbiota drive direct integration of phosphate stress and immunity. Nature 543, 513–518 (2017).
pubmed: 28297714 pmcid: 5364063 doi: 10.1038/nature21417
Bodenhausen, N., Bortfeld-Miller, M., Ackermann, M. & Vorholt, J. A. A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Genet. 10, e1004283 (2014).
pubmed: 24743269 pmcid: 3990490 doi: 10.1371/journal.pgen.1004283
Chen, T. et al. A plant genetic network for preventing dysbiosis in the phyllosphere. Nature 580, 653–657 (2020).
pubmed: 32350464 pmcid: 7197412 doi: 10.1038/s41586-020-2185-0
Horton, M. W. et al. Genome-wide association study of Arabidopsis thaliana leaf microbial community. Nat. Commun. 5, 5320 (2014).
pubmed: 25382143 doi: 10.1038/ncomms6320
Vorholt, J. A., Vogel, C., Carlstrom, C. I. & Müller, D. B. Establishing causality: opportunities of synthetic communities for plant microbiome research. Cell Host Microbe 22, 142–155 (2017).
pubmed: 28799900 doi: 10.1016/j.chom.2017.07.004
Bai, Y. et al. Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528, 364–369 (2015).
pubmed: 26633631 doi: 10.1038/nature16192
Durán, P. et al. Microbial interkingdom interactions in roots promote Arabidopsis survival. Cell 175, 973–983 (2018).
pubmed: 30388454 pmcid: 6218654 doi: 10.1016/j.cell.2018.10.020
Carlström, C. I. et al. Synthetic microbiota reveal priority effects and keystone strains in the Arabidopsis phyllosphere. Nat. Ecol. Evol. 3, 1445–1454 (2019).
pubmed: 31558832 pmcid: 6774761 doi: 10.1038/s41559-019-0994-z
Karasov, T. L. et al. The relationship between microbial population size and disease in the Arabidopsis thaliana phyllosphere. Preprint at bioRxiv https://doi.org/10.1101/828814 (2020).
Couto, D. & Zipfel, C. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16, 537–552 (2016).
pubmed: 27477127 doi: 10.1038/nri.2016.77
Peng, Y., van Wersch, R. & Zhang, Y. Convergent and divergent signaling in PAMP-triggered immunity and effector-triggered immunity. Mol. Plant Microbe Interact. 31, 403–409 (2018).
pubmed: 29135338 doi: 10.1094/MPMI-06-17-0145-CR
Torres, M. A., Dangl, J. L. & Jones, J. D. Arabidopsis gp91
pubmed: 11756663 doi: 10.1073/pnas.012452499
Gimenez-Ibanez, S., Ntoukakis, V. & Rathjen, J. P. The LysM receptor kinase CERK1 mediates bacterial perception in Arabidopsis. Plant Signal. Behav. 4, 539–541 (2009).
pubmed: 19816132 pmcid: 2688306 doi: 10.4161/psb.4.6.8697
Willmann, R. et al. Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc. Natl Acad. Sci. USA 108, 19824–19829 (2011).
pubmed: 22106285 pmcid: 3241766 doi: 10.1073/pnas.1112862108
Yamaguchi, Y., Huffaker, A., Bryan, A. C., Tax, F. E. & Ryan, C. A. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22, 508–522 (2010).
pubmed: 20179141 pmcid: 2845411 doi: 10.1105/tpc.109.068874
Xin, X. F. et al. Bacteria establish an aqueous living space in plants crucial for virulence. Nature 539, 524–529 (2016).
pubmed: 27882964 pmcid: 5135018 doi: 10.1038/nature20166
Staswick, P. E., Tiryaki, I. & Rowe, M. L. Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14, 1405–1415 (2002).
pubmed: 12084835 pmcid: 150788 doi: 10.1105/tpc.000885
Alonso, J. M., Hirayama, T., Roman, G., Nourizadeh, S. & Ecker, J. R. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284, 2148–2152 (1999).
pubmed: 10381874 doi: 10.1126/science.284.5423.2148
Clarke, J. D., Volko, S. M., Ledford, H., Ausubel, F. M. & Dong, X. Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell 12, 2175–2190 (2000).
pubmed: 11090217 pmcid: 150166 doi: 10.1105/tpc.12.11.2175
Tsuda, K., Sato, M., Stoddard, T., Glazebrook, J. & Katagiri, F. Network properties of robust immunity in plants. PLoS Genet. 5, e1000772 (2009).
pubmed: 20011122 pmcid: 2782137 doi: 10.1371/journal.pgen.1000772
Cao, H., Glazebrook, J., Clarke, J. D., Volko, S. & Dong, X. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88, 57–63 (1997).
pubmed: 9019406 doi: 10.1016/S0092-8674(00)81858-9
Mustilli, A.-C., Merlot, S., Vavasseur, A., Fenzi, F. & Giraudat, J. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14, 3089–3099 (2002).
pubmed: 12468729 pmcid: 151204 doi: 10.1105/tpc.007906
Bowling, S. A., Clarke, J. D., Liu, Y., Klessig, D. F. & Dong, X. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9, 1573–1584 (1997).
pubmed: 9338960 pmcid: 157034
Clarke, J. D., Liu, Y., Klessig, D. F. & Dong, X. Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell 10, 557–569 (1998).
pubmed: 9548982 pmcid: 144011 doi: 10.1105/tpc.10.4.557
Stegmann, M. et al. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355, 287–289 (2017).
pubmed: 28104890 doi: 10.1126/science.aal2541
Deslauriers, S. D. & Larsen, P. B. FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in Arabidopsis hypocotyls. Mol. Plant 3, 626–640 (2010).
pubmed: 20400488 doi: 10.1093/mp/ssq015
Suzuki, N. et al. Respiratory burst oxidases: the engines of ROS signaling. Curr. Opin. Plant Biol. 14, 691–699 (2011).
pubmed: 21862390 doi: 10.1016/j.pbi.2011.07.014
Torres, M. A. & Dangl, J. L. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr. Opin. Plant Biol. 8, 397–403 (2005).
pubmed: 15939662 doi: 10.1016/j.pbi.2005.05.014
Miller, G. et al. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2, ra45–ra45 (2009).
pubmed: 19690331 doi: 10.1126/scisignal.2000448
Zhang, J. et al. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1, 175–185 (2007).
pubmed: 18005697 doi: 10.1016/j.chom.2007.03.006
Qi, J., Wang, J., Gong, Z. & Zhou, J.-M. Apoplastic ROS signaling in plant immunity. Curr. Opin. Plant Biol. 38, 92–100 (2017).
pubmed: 28511115 doi: 10.1016/j.pbi.2017.04.022
Mersmann, S., Bourdais, G., Rietz, S. & Robatzek, S. Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiol. 154, 391–400 (2010).
pubmed: 20592040 pmcid: 2938167 doi: 10.1104/pp.110.154567
Denness, L. et al. Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis. Plant Physiol. 156, 1364–1374 (2011).
pubmed: 21546454 pmcid: 3135913 doi: 10.1104/pp.111.175737
Hamann, T., Bennett, M., Mansfield, J. & Somerville, C. Identification of cell-wall stress as a hexose-dependent and osmosensitive regulator of plant responses. The Plant J. 57, 1015–1026 (2009).
pubmed: 19036034 doi: 10.1111/j.1365-313X.2008.03744.x
Pogány, M. et al. Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis–Alternaria pathosystem. Plant Physiol. 151, 1459–1475 (2009).
pubmed: 19726575 pmcid: 2773049 doi: 10.1104/pp.109.141994
Fagard, M. et al. Arabidopsis thaliana expresses multiple lines of defense to counterattack Erwinia chrysanthemi. Mol. Plant Microbe Interact. 20, 794–805 (2007).
pubmed: 17601167 doi: 10.1094/MPMI-20-7-0794
Levy, M., Kolodziejczyk, A. A., Thaiss, C. A. & Elinav, E. Dysbiosis and the immune system. Nat. Rev. Immunol. 17, 219–232 (2017).
pubmed: 28260787 doi: 10.1038/nri.2017.7
Fryda, S. J. & Otta, J. D. Epiphytic movement and survival of Pseudomonas syringae on spring wheat. Phytopathology 68, 1064–1067 (1978).
doi: 10.1094/Phyto-68-1064
Tsuji, J., Somerville, S. C. & Hammerschmidt, R. Identification of a gene in Arabidopsis thaliana that controls resistance to Xanthomonas campestris pv campestris. Physiol. Mol. Plant Pathol. 38, 57–65 (1991).
doi: 10.1016/S0885-5765(05)80142-0
Obrien, R. D. & Lindow, S. E. Effect of plant-species and environmental-conditions on epiphytic population sizes of Pseudomonas syringae and other bacteria. Phytopathol. 79, 619–627 (1989).
doi: 10.1094/Phyto-79-619
Mew, T. W. & Kennedy, B. W. Seasonal variation in populations of pathogenic pseudomonads on soybean leaves. Phytopathol. 72, 103–105 (1982).
doi: 10.1094/Phyto-72-103
Jakob, K. et al. Pseudomonas viridiflava and P. syringae-natural pathogens of Arabidopsis thaliana. Mol. Plant Microbe Interact. 15, 1195–1203 (2002).
pubmed: 12481991 doi: 10.1094/MPMI.2002.15.12.1195
Ercolani, G. L. & Crosse, J. E. Growth of Pseudomonas phaseolicola and related plant pathogens in vivo. J. Gen. Microbiol. 45, 429–42 (1966).
doi: 10.1099/00221287-45-3-429
Morales, J., Kadota, Y., Zipfel, C., Molina, A. & Torres, M.-A. The Arabidopsis NADPH oxidases RbohD and RbohF display differential expression patterns and contributions during plant immunity. J. Exp. Bot. 67, 1663–1676 (2016).
pubmed: 26798024 doi: 10.1093/jxb/erv558
Kadota, Y. et al. Quantitative phosphoproteomic analysis reveals common regulatory mechanisms between effector- and PAMP-triggered immunity in plants. New Phytol. 221, 2160–2175 (2019).
pubmed: 30300945 doi: 10.1111/nph.15523
Li, L. et al. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15, 329–338 (2014).
pubmed: 24629339 doi: 10.1016/j.chom.2014.02.009
Kadota, Y. et al. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54, 43–55 (2014).
pubmed: 24630626 doi: 10.1016/j.molcel.2014.02.021
Lee, D. et al. Regulation of reactive oxygen species during plant immunity through phosphorylation and ubiquitination of RBOHD. Nat. Commun. 11, 1838 (2020).
pubmed: 32296066 pmcid: 7160206 doi: 10.1038/s41467-020-15601-5
Kimura, S. et al. CRK2 and C-terminal phosphorylation of NADPH oxidase RBOHD regulate reactive oxygen species production in Arabidopsis. Plant Cell 32, 1063–1080 (2020).
pubmed: 32034035 pmcid: 7145479 doi: 10.1105/tpc.19.00525
Sumimoto, H. Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J. 275, 3249–3277 (2008).
pubmed: 18513324 doi: 10.1111/j.1742-4658.2008.06488.x
Bedard, K. & Krause, K.-H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245–313 (2007).
pubmed: 17237347 doi: 10.1152/physrev.00044.2005
Grasberger, H. et al. Increased expression of DUOX2 is an epithelial response to mucosal dysbiosis required for immune homeostasis in mouse intestine. Gastroenterology 149, 1849–1859 (2015).
pubmed: 26261005 doi: 10.1053/j.gastro.2015.07.062
Sommer, F. & Bäckhed, F. The gut microbiota engages different signaling pathways to induce Duox2 expression in the ileum and colon epithelium. Mucosal Immunol. 8, 372–379 (2015).
pubmed: 25160818 doi: 10.1038/mi.2014.74
Flores, M. V. et al. Dual oxidase in the intestinal epithelium of zebrafish larvae has anti-bacterial properties. Biochem. Biophys. Res. Commun. 400, 164–168 (2010).
pubmed: 20709024 doi: 10.1016/j.bbrc.2010.08.037
Ha, E.-M., Oh, C.-T., Bae, Y. S. & Lee, W.-J. A direct role for dual oxidase in Drosophila gut immunity. Science 310, 847–850 (2005).
pubmed: 16272120 doi: 10.1126/science.1117311
Xiao, X. et al. A Mesh–Duox pathway regulates homeostasis in the insect gut. Nat. Microbiol. 2, 17020 (2017).
pubmed: 28248301 pmcid: 5332881 doi: 10.1038/nmicrobiol.2017.20
Winter, S. E. & Bäumler, A. J. Dysbiosis in the inflamed intestine. Gut Microbes 5, 71–73 (2014).
pubmed: 24637596 pmcid: 4049941 doi: 10.4161/gmic.27129
Halfvarson, J. et al. Dynamics of the human gut microbiome in inflammatory bowel disease. Nat. Microbiol. 2, 17004 (2017).
pubmed: 28191884 pmcid: 5319707 doi: 10.1038/nmicrobiol.2017.4
Kniskern, J. M., Traw, M. B. & Bergelson, J. Salicylic acid and jasmonic acid signaling defense pathways reduce natural bacterial diversity on Arabidopsis thaliana. Mol. Plant Microbe Interact. 20, 1512–1522 (2007).
pubmed: 17990959 doi: 10.1094/MPMI-20-12-1512
An, S.-Q. et al. Mechanistic insights into host adaptation, virulence and epidemiology of the phytopathogen Xanthomonas. FEMS Microbiol. Rev. 44, 1–32 (2019).
pmcid: 8042644 doi: 10.1093/femsre/fuz024
Bartoli, C. et al. In situ relationships between microbiota and potential pathobiota in Arabidopsis thaliana. ISME J. 12, 2024–2038 (2018).
pubmed: 29849170 pmcid: 6052059 doi: 10.1038/s41396-018-0152-7
Buell, C. R. Interactions between Xanthomonas species and Arabidopsis thaliana. Arabidopsis Book 1, e0031 (2002).
pubmed: 22303203 pmcid: 3243383 doi: 10.1199/tab.0031
Jacques, M.-A. et al. Using ecology, physiology, and genomics to understand host specificity in Xanthomonas. Annu. Rev. Phytopathol. 54, 163–187 (2016).
pubmed: 27296145 doi: 10.1146/annurev-phyto-080615-100147
Karasov, T. L. et al. Arabidopsis thaliana and Pseudomonas pathogens exhibit stable associations over evolutionary timescales. Cell Host Microbe 24, 168–179 (2018).
pubmed: 30001519 pmcid: 6054916 doi: 10.1016/j.chom.2018.06.011
Agler, M. T. et al. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol. 14, e1002352 (2016).
pubmed: 26788878 pmcid: 4720289 doi: 10.1371/journal.pbio.1002352
Essakhi, S. et al. Phylogenetic and variable-number tandem-repeat analyses identify nonpathogenic Xanthomonas arboricola lineages lacking the canonical type III secretion system. Appl. Environ. Microbiol. 81, 5395–5410 (2015).
pubmed: 26048944 pmcid: 4510168 doi: 10.1128/AEM.00835-15
Jochum, L. & Stecher, B. Label or concept—what is a pathobiont? Trends Microbiol. 28, 789–792 (2020).
pubmed: 32376073 doi: 10.1016/j.tim.2020.04.011
Helfrich, E. J. N. et al. Bipartite interactions, antibiotic production and biosynthetic potential of the Arabidopsis leaf microbiome. Nat.Microbiol. 3, 909–919 (2018).
pubmed: 30038309 pmcid: 7115891 doi: 10.1038/s41564-018-0200-0
Innerebner, G., Knief, C. & Vorholt, J. A. Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system. Appl. Environ. Microbiol. 77, 3202–3210 (2011).
pubmed: 21421777 pmcid: 3126462 doi: 10.1128/AEM.00133-11
Romero, F. M., Rossi, F. R., Gárriz, A., Carrasco, P. & Ruíz, O. A. A bacterial endophyte from apoplast fluids protects canola plants from different phytopathogens via antibiosis and induction of host resistance. Phytopathol. 109, 375–383 (2019).
doi: 10.1094/PHYTO-07-18-0262-R
Ritpitakphong, U. et al. The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen. New Phytol. 210, 1033–1043 (2016).
pubmed: 26725246 doi: 10.1111/nph.13808
Stromberg, K. D., Kinkel, L. L. & Leonard, K. J. Interactions between Xanthomonas translucens pv. translucens, the causal agent of bacterial leaf streak of wheat, and bacterial epiphytes in the wheat phyllosphere. Biol. Control 17, 61–72 (2000).
doi: 10.1006/bcon.1999.0771
Vogel, C., Bodenhausen, N., Gruissem, W. & Vorholt, J. A. The Arabidopsis leaf transcriptome reveals distinct but also overlapping responses to colonization by phyllosphere commensals and pathogen infection with impact on plant health. New Phytol. 212, 192–207 (2016).
pubmed: 27306148 doi: 10.1111/nph.14036
Berendsen, R. L. et al. Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J. 12, 1496–1507 (2018).
pubmed: 29520025 pmcid: 5956071 doi: 10.1038/s41396-018-0093-1
Yuan, M. et al. Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature 592, 105–109 (2021).
Ngou, B. P. M., Ahn, H.-K., Ding, P. & Jones, J. D. G. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature 592, 110–115 (2021).
Schlesier, B., Bréton, F. & Mock, H.-P. A hydroponic culture system for growing Arabidopsis thaliana plantlets under sterile conditions. Plant Mol. Biol. Rep. 21, 449–456 (2003).
doi: 10.1007/BF02772594
Chelius, M. K. & Triplett, E. W. The diversity of Archaea and Bacteria in association with the roots of Zea mays L. Microb. Ecol. 41, 252–263 (2001).
pubmed: 11391463 doi: 10.1007/s002480000087
Bulgarelli, D. et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95 (2012).
pubmed: 22859207 doi: 10.1038/nature11336
Reinhold-Hurek, B., Bünger, W., Burbano, C. S., Sabale, M. & Hurek, T. Roots shaping their microbiome: global hotspots for microbial activity. Annu. Rev. Phytopathol. 53, 403–424 (2015).
pubmed: 26243728 doi: 10.1146/annurev-phyto-082712-102342
Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinform. 26, 2460–2461 (2010).
doi: 10.1093/bioinformatics/btq461
Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013).
pubmed: 23955772 doi: 10.1038/nmeth.2604
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Gen. Biol. 15, 550 (2014).
doi: 10.1186/s13059-014-0550-8
de Mendiburu, F. & Yaseen, M. agricolae: statistical procedures for agricultural research. R package v.1.4.0 (R Foundation for Statistical Computing, 2020).
Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinform. 20, 289–290 (2004).
doi: 10.1093/bioinformatics/btg412
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag, 2009).
Oksanen, F. et al. vegan: community ecology package. R package v.2.5-6 (R Foundation for Statistical Computing, 2019).
Pruesse, E., Peplies, J. & Glöckner, F. O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinform. 28, 1823–1829 (2012).
doi: 10.1093/bioinformatics/bts252
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).
pubmed: 20525638 doi: 10.1093/sysbio/syq010
Pfeilmeier, S., Saur, I. M.-L., Rathjen, J. P., Zipfel, C. & Malone, J. G. High levels of cyclic-di-GMP in plant-associated Pseudomonas correlate with evasion of plant immunity. Mol. Plant Pathol. 17, 521–531 (2016).
pubmed: 26202381 doi: 10.1111/mpp.12297

Auteurs

Sebastian Pfeilmeier (S)

Institute of Microbiology, ETH Zurich, Zurich, Switzerland.

Gabriella C Petti (GC)

Institute of Microbiology, ETH Zurich, Zurich, Switzerland.

Miriam Bortfeld-Miller (M)

Institute of Microbiology, ETH Zurich, Zurich, Switzerland.

Benjamin Daniel (B)

Institute of Microbiology, ETH Zurich, Zurich, Switzerland.

Christopher M Field (CM)

Institute of Microbiology, ETH Zurich, Zurich, Switzerland.

Shinichi Sunagawa (S)

Institute of Microbiology, ETH Zurich, Zurich, Switzerland.

Julia A Vorholt (JA)

Institute of Microbiology, ETH Zurich, Zurich, Switzerland. jvorholt@ethz.ch.

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Genome, Viral Ralstonia Composting Solanum lycopersicum Bacteriophages

Classifications MeSH