Universität zu Köln

Uhlmann, Charles ORCID: 0000-0002-6749-4805 (2023). Analysis of Arabidopsis thaliana glucosinolate profiles in response to a native root fungal endophyte. PhD thesis, Universität zu Köln.

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Abstract

Plants host communities of microbes termed the microbiota, which contributes to plant nutrition and stress relief, notably in roots. With diverse microbiota fungi, plants can accept invasive hyphal growth inside their cells. Which immune signaling pathways regulate colonization of root tissues and cells by fungal endophytes is unclear. However, at the metabolite level, Tryptophan (Trp)-derived compounds, including indolic-glucosinolates (GLS), prevent excessive fungal endophyte growth and associated harm in roots of Arabidopsis thaliana (Arabidopsis). This PhD thesis aims to provide i) knowledge on immune pathways relevant to general fungal colonization and ii) insights into the regulation of aliphatic- and indolic-GLS by phosphate (Pi). In the first chapter, I explored whether the broad host range Sebacinales fungi showed enhanced or reduced growth in roots of diverse established Arabidopsis immunity mutants but detected no differences compared to wild-type Col-0 plants. In the second chapter, I investigated whether the Phosphate Starvation Response (PSR) system modulates aliphatic and indolic-GLS accumulation as important immune metabolic outputs. As fungal endophyte test organism, I selected a strain of Truncatella angustata (F73) isolated from Arabidopsis roots in nature and known to relieve long-term Pi limitation stress in an agar-based system. Using confocal microscopy, I determined that the root differentiation zone is more permissive to rapid F73 intracellular colonization, compared to the root apical meristem or the elongation zone. A fluorescent transcriptional reporter of the Trp-derived metabolites pathway showed increased signal width in the differentiation zone upon F73 inoculation, suggesting Arabidopsis responds to fungal colonization by spatially expanding Trp-derived metabolite production. I then performed time course RNA-seq and GLS quantification experiments to reveal how Pi and immune signaling are integrated at the transcriptional and metabolomics levels. Pi availability did not impact GLS-related gene expression but governed the number of F73-responsive genes in Col-0 in a temporal manner, suggesting that the PSR regulates general immune dynamics. Yet, amounts of long chained aliphatic-GLS in roots and shoots were constitutively higher at low Pi. Furthermore, F73 induced greater accumulation of most GLS at high Pi, hinting at PSR dependent modulation of GLS synthesis. F73 displayed hallmarks of increased growth rate and virulence at a transcriptional level, but not deleterious infection, in the cyp79b2/b3 mutant depleted in Trp-derived metabolites. Altogether, my work provides spatio-temporal insights into how Pi stress influences interactions with fungi and suggests that the PSR fine-tunes aliphatic- and indolic-GLS accumulation. This hypothesis warrants further exploration using PSR mutants.

Item Type:	Thesis (PhD thesis)
Translated title:	Title Language Analyse der Glucosinolatprofile von Arabidopsis thaliana Glucosinolatprofilen als Reaktion auf einen einheimischen Wurzelpilz-Endophyt German
Translated abstract:	Abstract Language Pflanzen beherbergen Gemeinschaften von Mikroben, die so genannte Mikrobiota, die zur Ernährung der Pflanzen und zum Stressabbau beitragen, insbesondere in den Wurzeln. Verschiedene Pflanzen-assoziierte Pilze können Pflanzenzellen invasiv mit ihren Hyphen besiedeln. Welche Immunsignalwege die Besiedlung von Wurzelgeweben und -zellen durch Pilzendophyten regulieren, ist unklar. Auf der Metabolitebene, verhindern Tryptophan (Trp)- abgeleitete Verbindungen, darunter Indol-Glucosinolate (GLS), ein übermäßiges Wachstum von Pilz-Endophyten und damit verbundene Schäden in den Wurzeln von Arabidopsis thaliana (Arabidopsis). Ziel dieser Dissertation ist es, i) Erkenntnisse über Immunsignalwege zu gewinnen, die für die Pilzbesiedlung relevant sind, und ii) Einblicke in die Regulierung von aliphatischen und indolischen GLS zu gewinnen. Ich untersuchte, ob Pilze der Ordnung Sebacinales, welche durch ein breites Wirtsspektrum gekennzeichnet sind, in den Wurzeln verschiedener etablierter Arabidopsis-Immunitätsmutanten ein verstärktes oder reduziertes Wachstum zeigten, konnte jedoch keine Unterschiede im Vergleich zu Wildtyp-Pflanzen des Ecotyps Col-0 feststellen. Anschließend untersuchte ich, ob das Phosphatmangel-Reaktions (PSR) System des Wirtes die Akkumulation von aliphatischen und indolischen GLS als wichtige immunologische Stoffwechselprodukte moduliert. Als Pilz-Endophyt-Testorganismus wählte ich einen Stamm von Truncatella angustata (F73), der in der Natur aus Arabidopsis- Wurzeln isoliert wurde und dafür bekannt ist, dass er in einem agarbasierten System langfristigen Phosphat-(Pi)-Limitierungsstress beseitigt. Mit Hilfe der konfokalen Mikroskopie habe ich festgestellt, dass die Wurzeldifferenzierungszone für eine schnelle intrazelluläre Besiedlung durch F73 durchlässiger ist als das Wurzelapikalmeristem oder die Streckungszone. Als nächstes zeigte ein fluoreszierender Transkriptionsreporter des Trp-Stoffwechselwegs eine erhöhte Signalbreite in der Differenzierungszone bei F73-Inokulation, was darauf hindeutet, dass Arabidopsis auf die Pilzbesiedlung mit einer räumlichen Ausweitung der Produktion von Trp-Stoffwechselprodukten reagiert. Anschließend führte ich Zeitverlaufs-RNA-seq- und GLSQuantifizierungsexperimente durch, um herauszufinden, wie Pi und die Immunsignalisierung auf der Transkriptions- und Metabolomebene integriert sind. Die Pi-Verfügbarkeit wirkte sich nicht auf die GLS-bezogene Genexpression aus, steuerte aber die Anzahl der auf F73 reagierenden Gene in Col-0 in zeitlicher Abhängigkeit, was darauf hindeutet, dass die PSR die allgemeine Immundynamik reguliert. Die GLS-Quantifizierung zeigte dennoch, dass die Mengen an langkettigen aliphatischen GLS in Wurzeln und Sprossen bei niedrigem Pi konstitutiv höher waren. Darüber hinaus induzierte F73 eine stärkere Akkumulation der meisten GLS bei hohem Pi, was auf eine PSR-abhängige Modulation der GLS-Synthese hindeutet. F73 zeigte in der cyp79b2/b3-Mutante, welche durch eine gestörte Produktion von Trp-abgeleiteten Metaboliten charakterisiert ist, Merkmale einer erhöhten Wachstumsrate und Virulenz auf transkriptioneller Ebene, aber keine schädliche Infektion des Wirtes. Insgesamt bietet meine Arbeit räumlich-zeitliche Einblicke in die Art und Weise, wie Pi-Stress die pflanzliche Interaktionen mit Pilzen beeinflusst, und legt nahe, dass die PSR die Akkumulation aliphatischer und indolischer GLS moduliert. Diese Hypothese sollte mit Hilfe von PSRMutanten weiter erforscht werden. German
Creators:	Creators Email ORCID ORCID Put Code Uhlmann, Charles UNSPECIFIED orcid.org/0000-0002-6749-4805 UNSPECIFIED
Contributors:	Contribution Name Email Thesis advisor Parker, Jane parker@mpipz.mpg.de
URN:	urn:nbn:de:hbz:38-655738
Date:	4 May 2023
Place of Publication:	KUPS
Language:	English
Faculty:	Faculty of Mathematics and Natural Sciences
Divisions:	Außeruniversitäre Forschungseinrichtungen > MPI for Plant Breeding Research
Subjects:	Life sciences
Uncontrolled Keywords:	Keywords Language Glucosinolate English Phosphate Starvation Response English Fungal endophyte English
Date of oral exam:	27 February 2023
Referee:	Name Academic Title Parker, Jane Dr.
References:	Albert I, Böhm H, Albert M, Feiler CE, Imkampe J, Wallmeroth N, Brancato C, Raaymakers TM, Oome S, Zhang H, Krol E, Grefen C, Gust AA, Chai J, Hedrich R, Van Den Ackerveken G & Nürnberger T (2015) An RLP23-SOBIR1-BAK1 complex mediates NLP-triggered immunity. Nat. Plants 1: 1–9 Anthony MA, Celenza JL, Armstrong A & Frey SD (2020) Indolic glucosinolate pathway provides resistance to mycorrhizal fungal colonization in a non-host Brassicaceae. Ecosphere 11: Attard A, Gourgues M, Callemeyn-Torre N & Keller H (2010) The immediate activation of defense responses in Arabidopsis roots is not sufficient to prevent Phytophthora parasitica infection. New Phytol. 187: 449–460 Baggs EL, Monroe JG, Thanki AS, O’Grady R, Schudoma C, Haerty W & Krasileva K V. (2020) Convergent loss of an EDS1/PAD4 signaling pathway in several plant lineages reveals coevolved components of plant immunity and drought response. Plant Cell 32: 2158–2177 Balzergue C, Puech-Pags V, Bécard G & Rochange SF (2011) The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. J. Exp. Bot. 62: 1049–1060 Available at: https://academic.oup.com/jxb/articlelookup/ doi/10.1093/jxb/erq335 [Accessed April 9, 2018] Barragán-Rosillo AC, Peralta-Alvarez CA, Ojeda-Rivera JO, Arzate-Mejía RG, Recillas- Targa F & Herrera-Estrella L (2021) Genome accessibility dynamics in response to phosphate limitation is controlled by the PHR1 family of transcription factors in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 118: Bennett AE & Groten K (2022) The Costs and Benefits of Plant-Arbuscular Mycorrhizal Fungal Interactions. Annu. Rev. Plant Biol. 73: 649–672 Berens ML, Wolinska KW, Spaepen S, Ziegler J, Nobori T, Nair A, Krüler V, Winkelmüller TM, Wang Y, Mine A, Becker D, Garrido-Oter R, Schulze-Lefert P & Tsuda K (2019) Balancing trade-offs between biotic and abiotic stress responses through leaf agedependent variation in stress hormone cross-talk. Proc. Natl. Acad. Sci. U. S. A. 116: 2364–2373 Bhandari DD, Lapin D, Kracher B, von Born P, Bautor J, Niefind K & Parker JE (2019) An EDS1 heterodimer signalling surface enforces timely reprogramming of immunity genes in Arabidopsis. Nat. Commun. 10: 772 Available at: http://www.nature.com/articles/s41467-019-08783-0 [Accessed May 6, 2019] Bolger AM, Lohse M & Usadel B (2014) Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114–2120 Böttcher C, Westphal L, Schmotz C, Prade E, Scheel D & Glawischnig E (2009) The multifunctional enzyme CYP71b15 (Phytoalexin deficient3) converts cysteine-lndole-3- acetonitrile to camalexin in the lndole-3-acetonitrile metabolic network of arabidopsis thaliana. Plant Cell 21: 1830–1845 Bozkurt TO & Kamoun S (2020) The plant–pathogen haustorial interface at a glance. J. Cell Sci. 133: jcs237958 Available at: http://jcs.biologists.org/lookup/doi/10.1242/jcs.237958 Bravo A, York T, Pumplin N, Mueller LA & Harrison MJ (2016) Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics. Nat. Plants 2: 15208 Available at: http://www.nature.com/articles/nplants2015208 [Accessed May 26, 2018] Brundrett MC & Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol. Available at: http://doi.wiley.com/10.1111/nph.14976 Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, Pérez-Pérez J, Solano R, Leyva A & Paz-Ares J (2010) A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in arabidopsis. PLoS Genet. 6: Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP, Joachimiak A & Stacey G (2014) The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. Elife 3: 1–19 Castrillo G, Teixeira PJPL, Paredes SH, Law TF, de Lorenzo L, Feltcher ME, Finkel OM, Breakfield NW, Mieczkowski P, Jones CD, Paz-Ares J & Dangl JL (2017) Root microbiota drive direct integration of phosphate stress and immunity. Nature 543: 513– 518 Available at: https://doi.org/10.1038/nature21417 Clark RM, Schweikert G, Toomajian C, Ossowski S, Zeller G, Shinn P, Warthmann N, Hu TT, Fu G, Hinds DA, Chen H, Frazer KA, Huson DH, Scholkopf B, Nordborg M, Ratsch G, Ecker JR & Weigel D (2007) Common Sequence Polymorphisms Shaping Genetic Diversity in Arabidopsis thaliana. Science (80-. ). 317: 338–342 Available at: http://science.sciencemag.org/content/317/5836/338.abstract Clay NK, Adio AM, Denoux C, Jander G & Ausubel FM (2009) Glucosinolate Metabolites Required for an Arabidopsis Innate Immune Response. Science (80-. ). 323: 95–101 Available at: https://www.science.org/doi/10.1126/science.1164627 Cui H, Tsuda K & Parker JE (2015) Effector-Triggered Immunity: From Pathogen Perception to Robust Defense. Annu. Rev. Plant Biol. 66: 487–511 Available at: http://www.annualreviews.org/doi/10.1146/annurev-arplant-050213-040012 [Accessed October 16, 2018] Das D, Paries M, Hobecker K, Gigl M, Dawid C, Lam H-M, Zhang J, Chen M & Gutjahr C (2022) PHOSPHATE STARVATION RESPONSE transcription factors enable arbuscular mycorrhiza symbiosis. Nat. Commun. 13: 477 Available at: https://www.nature.com/articles/s41467-022-27976-8 Delaux P-M, Radhakrishnan G V., Jayaraman D, Cheema J, Malbreil M, Volkening JD, Sekimoto H, Nishiyama T, Melkonian M, Pokorny L, Rothfels CJ, Sederoff HW, Stevenson DW, Surek B, Zhang Y, Sussman MR, Dunand C, Morris RJ, Roux C, Wong GK-S, et al (2015) Algal ancestor of land plants was preadapted for symbiosis. Proc. Natl. Acad. Sci. 112: 13390–13395 Available at: http://www.pnas.org/lookup/doi/10.1073/pnas.1515426112 Deslandes L & Rivas S (2012) Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17: 644–655 Available at: https://www.sciencedirect.com/science/article/pii/S1360138512001495?via%3Dihub#fig 0005 [Accessed May 9, 2019] Durán P, Thiergart T, Garrido-Oter R, Agler M, Kemen E, Schulze-Lefert P & Hacquard S (2018) Microbial Interkingdom Interactions in Roots Promote Arabidopsis Survival. Cell 175: 973–983.e14 Available at: http://www.ncbi.nlm.nih.gov/pubmed/30388454 [Accessed November 7, 2018] Emonet A, Zhou F, Vacheron J, Heiman CM, Dénervaud Tendon V, Ma KW, Schulze-Lefert P, Keel C & Geldner N (2021) Spatially Restricted Immune Responses Are Required for Maintaining Root Meristematic Activity upon Detection of Bacteria. Curr. Biol. 31: 1012–1028.e7 Feng F, Sun J, Radhakrishnan G V., Lee T, Bozsóki Z, Fort S, Gavrin A, Gysel K, Thygesen MB, Andersen KR, Radutoiu S, Stougaard J & Oldroyd GED (2019) A combination of chitooligosaccharide and lipochitooligosaccharide recognition promotes arbuscular mycorrhizal associations in Medicago truncatula. Nat. Commun. 10: 5047 Available at: http://www.nature.com/articles/s41467-019-12999-5 [Accessed November 23, 2019] Frerigmann H, Piotrowski M, Lemke R, Bednarek P & Schulze-Lefert P (2021) A network of phosphate starvation and immune-related signaling and metabolic pathways controls the interaction between arabidopsis thaliana and the beneficial fungus colletotrichum tofieldiae. Mol. Plant-Microbe Interact. 34: 560–570 Frerigmann H, Piślewska-Bednarek M, Sánchez-Vallet A, Molina A, Glawischnig E, Gigolashvili T & Bednarek P (2016) Regulation of Pathogen-Triggered Tryptophan Metabolism in Arabidopsis thaliana by MYB Transcription Factors and Indole Glucosinolate Conversion Products. Mol. Plant 9: 682–695 Gan T, Luo T, Pang K, Zhou C, Zhou G, Wan B, Li G, Yi Q, Czaja AD & Xiao S (2021) Cryptic terrestrial fungus-like fossils of the early Ediacaran Period. Nat. Commun. 12: Available at: http://dx.doi.org/10.1038/s41467-021-20975-1 Gao M, Zhang C, Angel W, Kwak O, Allison J, Wiratan L, Hallworth A, Wolf J & Lu H (2022) Circadian Regulation of the GLYCINE-RICH RNA-BINDING PROTEIN Gene by the Master Clock Protein CIRCADIAN CLOCK-ASSOCIATED 1 Is Important for Plant Innate Immunity . J. Exp. Bot.: 1–13 Gao YQ, Bu LH, Han ML, Wang YL, Li ZY, Liu HT & Chao DY (2021) Long-distance blue light signalling regulates phosphate deficiency-induced primary root growth inhibition. Mol. Plant 14: 1539–1553 Available at: https://doi.org/10.1016/j.molp.2021.06.002 Grigoriev I V., Nikitin R, Haridas S, Kuo A, Ohm R, Otillar R, Riley R, Salamov A, Zhao X, Korzeniewski F, Smirnova T, Nordberg H, Dubchak I & Shabalov I (2014) MycoCosm portal: Gearing up for 1000 fungal genomes. Nucleic Acids Res. 42: 699–704 Gu Z, Eils R & Schlesner M (2016) Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32: 2847–2849 Guan R, Su J, Meng X, Li S, Liu Y, Xu J & Zhang S (2015) Multilayered regulation of ethylene induction plays a positive role in arabidopsis resistance against Pseudomonas syringae. Plant Physiol. 169: 299–312 Harbort CJ, Hashimoto M, Inoue H, Niu Y, Guan R, Rombolà AD, Kopriva S, Voges MJEEE, Sattely ES, Garrido-Oter R & Schulze-Lefert P (2020) Root-Secreted Coumarins and the Microbiota Interact to Improve Iron Nutrition in Arabidopsis. Cell Host Microbe 28: 825–837.e6 Available at: https://linkinghub.elsevier.com/retrieve/pii/S1931312820305072 Harun S, Abdullah-Zawawi MR, Goh HH & Mohamed-Hussein ZA (2020) A Comprehensive Gene Inventory for Glucosinolate Biosynthetic Pathway in Arabidopsis thaliana. J. Agric. Food Chem. 68: 7281–7297 Hassani MA, Durán P & Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6: 58 Available at: https://microbiomejournal.biomedcentral.com/articles/10.1186/s40168-018-0445-0 [Accessed August 13, 2018] Van Der Heijden MGA, Bruin S De, Luckerhoff L, Van Logtestijn RSP & Schlaeppi K (2016) A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. ISME J. 10: 389–399 Available at: http://dx.doi.org/10.1038/ismej.2015.120 Hindt MN, Akmakjian GZ, Pivarski KL, Punshon T, Baxter I, Salt DE & Guerinot M Lou (2017) BRUTUS and its paralogs, BTS LIKE1 and BTS LIKE2, encode important negative regulators of the iron deficiency response in Arabidopsis thaliana. Metallomics 9: 876–890 Hiruma K, Fukunaga S, Bednarek P, Piślewska-Bednarek M, Watanabe S, Narusaka Y, Shirasu K & Takano Y (2013) Glutathione and tryptophan metabolism are required for Arabidopsis immunity during the hypersensitive response to hemibiotrophs. Proc. Natl. Acad. Sci. U. S. A. 110: 9589–9594 Hiruma K, Gerlach N, Sacristán S, Nakano RT, Hacquard S, Kracher B, Neumann U, Ramírez D, Bucher M, O’Connell RJ & Schulze-Lefert P (2016) Root Endophyte Colletotrichum tofieldiae Confers Plant Fitness Benefits that Are Phosphate Status Dependent. Cell 165: 464–474 Available at: http://www.ncbi.nlm.nih.gov/pubmed/26997485 [Accessed May 26, 2018] Hu D, Zhang S, Baskin JM, Baskin CC, Wang Z, Liu R, Du J, Yang X & Huang Z (2019) Seed mucilage interacts with soil microbial community and physiochemical processes to affect seedling emergence on desert sand dunes. Plant Cell Environ. 42: 591–605 Ivanov S, Austin J, Berg RH & Harrison MJ (2019) Extensive membrane systems at the host– arbuscular mycorrhizal fungus interface. Nat. Plants 5: 194–203 Available at: http://www.nature.com/articles/s41477-019-0364-5 Jang G, Yoon Y & Choi Y Do (2020) Crosstalk with jasmonic acid integrates multiple responses in plant development. Int. J. Mol. Sci. 21: 1–15 Kadota Y, Liebrand TWH, Goto Y, Sklenar J, Derbyshire P, Menke FLH, Torres MA, Molina A, Zipfel C, Coaker G & Shirasu K (2019) Quantitative phosphoproteomic analysis reveals common regulatory mechanisms between effector- and PAMP-triggered immunity in plants. New Phytol. 221: 2160–2175 Available at: https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.15523 [Accessed April 29, 2019] Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M & Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol. Biochem. 41: 1233–1244 Available at: http://dx.doi.org/10.1016/j.soilbio.2009.03.005 Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J & Bücking H (2011) Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis. Science (80-. ). 333: 880–882 Available at: https://doi.org/10.1126/science.1208473 Kim D, Paggi JM, Park C, Bennett C & Salzberg SL (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37: 907–915 Available at: http://dx.doi.org/10.1038/s41587-019-0201-4 Klein M, Reichelt M, Gershenzon J & Papenbrock J (2006) The three desulfoglucosinolate sulfotransferase proteins in Arabidopsis have different substrate specificities and are differentially expressed. FEBS J. 273: 122–136 Kliebenstein DJ, D’Auria JC, Behere AS, Kim JH, Gunderson KL, Breen JN, Lee G, Gershenzon J, Last RL & Jander G (2007) Characterization of seed-specific benzoyloxyglucosinolate mutations in Arabidopsis thaliana. Plant J. 51: 1062–1076 Koh S, André A, Edwards H, Ehrhardt D & Somerville S (2005) Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J. 44: 516–529 Kremer JM, Sohrabi R, Paasch BC, Rhodes D, Thireault C, Schulze-Lefert P, Tiedje JM & He SY (2021) Peat-based gnotobiotic plant growth systems for Arabidopsis microbiome research. Nat. Protoc. 16: 2450–2470 Available at: http://dx.doi.org/10.1038/s41596- 021-00504-6 Krings M, Taylor TN, Hass H, Kerp H, Dotzler N & Hermsen EJ (2007) Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytol. 174: 648–657 Available at: http://doi.wiley.com/10.1111/j.1469- 8137.2007.02008.x Kuchernig JC, Burow M & Wittstock U (2012) Evolution of specifier proteins in glucosinolate-containing plants. BMC Evol. Biol. 12: Lahrmann U, Ding Y, Banhara A, Rath M, Hajirezaei MR, Döhlemann S, von Wirén N, Parniske M & Zuccaro A (2013) Host-related metabolic cues affect colonization strategies of a root endophyte. Proc. Natl. Acad. Sci. 110: 13965–13970 Available at: http://www.ncbi.nlm.nih.gov/pubmed/23918389 [Accessed October 16, 2018] Lahrmann U, Strehmel N, Langen G, Frerigmann H, Leson L, Ding Y, Scheel D, Herklotz S, Hilbert M & Zuccaro A (2015) Mutualistic root endophytism is not associated with the reduction of saprotrophic traits and requires a noncompromised plant innate immunity. New Phytol. 207: 841–857 Available at: http://doi.wiley.com/10.1111/nph.13411 [Accessed October 16, 2018] Leek JT, Johnson WE, Parker HS, Jaffe AE & Storey JD (2012) The SVA package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics 28: 882–883 Li C, Zhang Q, Xia Y & Jin K (2021) MaNmra, a negative transcription regulator in nitrogen catabolite repression pathway, contributes to nutrient utilization, stress resistance, and virulence in entomopathogenic fungus metarhizium acridum. Biology (Basel). 10: 1167 Available at: https://www.mdpi.com/2079-7737/10/11/1167 Liang Y, Cao Y, Tanaka K, Thibivilliers S, Wan J, Choi J, Kang C ho, Qiu J & Stacey G (2013) Nonlegumes respond to rhizobial nod factors by suppressing the innate immune response. Science (80-. ). 341: 1384–1387 Available at: http://www.ncbi.nlm.nih.gov/pubmed/24009356 [Accessed February 27, 2019] Liao Y, Smyth GK & Shi W (2014) FeatureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30: 923–930 Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F, Molina A, Parker J, Somerville S & Schulze-Lefert P (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310: 1180–3 Available at: http://www.ncbi.nlm.nih.gov/pubmed/16293760 [Accessed February 13, 2019] Liu L, Sonbol FM, Huot B, Gu Y, Withers J, Mwimba M, Yao J, He SY & Dong X (2016) Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effector-triggered immunity. Nat. Commun. 7: 1–10 Available at: http://dx.doi.org/10.1038/ncomms13099 Liu T, Liu Z, Song C, Hu Y, Han Z, She J, Fan G, Wang J, Jin C, Chang J, Zhou JM & Chai J (2012) Chitin-induced dimerization activates a plant immune receptor. Science (80-. ). 336: 1160–1164 Love MI, Huber W & Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15: 1–21 Lu Y & Tsuda K (2021) Intimate Association of PRR- and NLR-Mediated Signaling in Plant Immunity. Mol. Plant. Microbe. Interact. 34: 3–14 Luginbuehl LH, Menard GN, Kurup S, Van Erp H, Radhakrishnan G V., Breakspear A, Oldroyd GED & Eastmond P (2017) Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science (80-. ). 356: 1175–1176 Luginbuehl LH & Oldroyd GED (2017) Understanding the Arbuscule at the Heart of Endomycorrhizal Symbioses in Plants. Curr. Biol. 27: R952–R963 Available at: http://dx.doi.org/10.1016/j.cub.2017.06.042 Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: Tools for future crops. Plant Physiol. 156: 1041–1049 Ma L, Shi Y, Siemianowski O, Yuan B, Egner TK, Mirnezami SV, Lind KR, Ganapathysubramanian B, Venditti V & Cademartiri L (2019) Hydrogel-based transparent soils for root phenotyping in vivo. Proc. Natl. Acad. Sci. U. S. A. 166: 11063–11068 Ma Z, Guo D, Xu X, Lu M, Bardgett RD, Eissenstat DM, McCormack ML & Hedin LO (2018) Evolutionary history resolves global organization of root functional traits. Nature 555: 94–97 Available at: http://www.nature.com/doifinder/10.1038/nature25783 [Accessed January 31, 2019] Maciá-Vicente JG, Bai B, Qi R, Ploch S, Breider F & Thines M (2022) Nutrient Availability Does Not Affect Community Assembly in Root-Associated Fungi but Determines Fungal Effects on Plant Growth. mSystems 7: Meier K, Ehbrecht MD & Wittstock U (2019) Glucosinolate Content in Dormant and Germinating Arabidopsis thaliana Seeds Is Affected by Non-Functional Alleles of Classical Myrosinase and Nitrile-Specifier Protein Genes. Front. Plant Sci. 10: 1–14 Menand B, Yi K, Jouannic S, Hoffmann L, Ryan E, Linstead P, Schaefer DG & Dolan L (2007) An Ancient Mechanism Controls the Development of Cells with a Rooting Function in Land Plants. Science (80-. ). 316: 1477–1480 Available at: http://www.ncbi.nlm.nih.gov/pubmed/17556585 [Accessed December 8, 2017] Meschke H & Schrempf H (2010) Streptomyces lividans inhibits the proliferation of the fungus Verticillium dahliae on seeds and roots of Arabidopsis thaliana. Microb. Biotechnol. 3: 428–443 Mesny F, Miyauchi S, Thiergart T, Pickel B, Atanasova L, Karlsson M, Hüttel B, Barry KW, Haridas S, Chen C, Bauer D, Andreopoulos W, Pangilinan J, LaButti K, Riley R, Lipzen A, Clum A, Drula E, Henrissat B, Kohler A, et al (2021) Genetic determinants of endophytism in the Arabidopsis root mycobiome. Nat. Commun. 12: 1–15 Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, Werck-Reichhart D & Ausubel FM (2010) Innate Immune Responses Activated in Arabidopsis Roots by Microbe97 PhD dissertation C. Uhlmann Associated Molecular Patterns. Plant Cell 22: 973–990 Available at: https://academic.oup.com/plcell/article/22/3/973/6096733 Mithen R, Bennett R & Marquez J (2010) Glucosinolate biochemical diversity and innovation in the Brassicales. Phytochemistry 71: 2074–2086 Available at: http://dx.doi.org/10.1016/j.phytochem.2010.09.017 Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H & Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. 104: 19613–19618 Available at: http://www.ncbi.nlm.nih.gov/pubmed/18042724 [Accessed January 22, 2019] Newman A, Picot E, Davies S, Hilton S, Carré IA & Bending GD (2022) Circadian rhythms in the plant host influence rhythmicity of rhizosphere microbiota. BMC Biol. 20: 1–15 Available at: https://doi.org/10.1186/s12915-022-01430-z Ngou BPM, Ahn HK, Ding P & Jones JDG (2021) Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature 592: 110–115 Nishiyama T, Sakayama H, de Vries J, Buschmann H, Saint-Marcoux D, Ullrich KK, Haas FB, Vanderstraeten L, Becker D, Lang D, Vosolsobě S, Rombauts S, Wilhelmsson PKI, Janitza P, Kern R, Heyl A, Rümpler F, Villalobos LIAC, Clay JM, Skokan R, et al (2018) The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization. Cell 174: 448–464.e24 Available at: https://linkinghub.elsevier.com/retrieve/pii/S0092867418308018 Nongbri PL, Johnson JM, Sherameti I, Glawischnig E, Halkier BA & Oelmüller R (2012) Indole-3-Acetaldoxime-Derived Compounds Restrict Root Colonization in the Beneficial Interaction Between Arabidopsis Roots and the Endophyte Piriformospora indica. Mol. Plant-Microbe Interact. 25: 1186–1197 Available at: http://apsjournals.apsnet.org/doi/10.1094/MPMI-03-12-0071-R [Accessed February 7, 2019] O’Connell RJ & Panstruga R (2006) Tête à tête inside a plant cell: Establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol. 171: 699–718 Oba H, Tawaray K & Wagatsuma T (2001) Arbuscular mycorrhizal colonization in Lupinus and related genera. Soil Sci. Plant Nutr. 47: 685–694 Available at: http://www.tandfonline.com/doi/abs/10.1080/00380768.2001.10408433 [Accessed May 26, 2018] Pant B-D, Pant P, Erban A, Huhman D, Kopka J & Scheible W-R (2015) Identification of primary and secondary metabolites with phosphorus status-dependent abundance in Arabidopsis, and of the transcription factor PHR1 as a major regulator of metabolic changes during phosphorus limitation. Plant. Cell Environ. 38: 172–87 Available at: https://onlinelibrary.wiley.com/doi/10.1111/pce.12378 Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Micro 6: 763–775 Available at: https://www.nature.com/nrmicro/journal/v6/n10/full/nrmicro1987.html [Accessed May 22, 2017] Peng J, Aluthmuhandiram JVS, Chethana KWT, Zhang Q, Xing Q, Wang H, Liu M, Zhang W, Li X & Yan J (2022) An NmrA-Like Protein, Lws1, Is Important for Pathogenesis in the Woody Plant Pathogen Lasiodiplodia theobromae. Plants 11: 2197 Available at: https://www.mdpi.com/2223-7747/11/17/2197 Lo Presti L, Lanver D, Schweizer G, Tanaka S, Liang L, Tollot M, Zuccaro A, Reissmann S & Kahmann R (2015) Fungal Effectors and Plant Susceptibility. Annu. Rev. Plant Biol. 66: 513–545 Available at: http://www.annualreviews.org/doi/10.1146/annurev-arplant- 043014-114623 Proust H, Honkanen S, Jones VAS, Morieri G, Prescott H, Kelly S, Ishizaki K, Kohchi T & Dolan L (2016) RSL Class i Genes Controlled the Development of Epidermal Structures in the Common Ancestor of Land Plants. Curr. Biol. 26: 93–99 Available at: http://linkinghub.elsevier.com/retrieve/pii/S0960982215014360 [Accessed December 8, 2017] Pruitt RN, Locci F, Wanke F, Zhang L, Saile SC, Joe A, Karelina D, Hua C, Fröhlich K, Wan WL, Hu M, Rao S, Stolze SC, Harzen A, Gust AA, Harter K, Joosten MHAJ, Thomma BPHJ, Zhou JM, Dangl JL, et al (2021) The EDS1–PAD4–ADR1 node mediates Arabidopsis pattern-triggered immunity. Nature 598: 495–499 Qin L, Zhou Z, Li Q, Zhai C, Liu L, Quilichini TD, Gao P, Kessler SA, Jaillais Y, Datla R, Peng G, Xiang D & Wei Y (2020) Specific recruitment of phosphoinositide species to the plant-pathogen interfacial membrane underlies Arabidopsis susceptibility to fungal infection. Plant Cell 32: 1665–1688 Rajniak J, Barco B, Clay NK & Sattely ES (2015) A new cyanogenic metabolite in Arabidopsis required for inducible pathogen defence. Nature 525: 376–379 Redecker D (2000) Glomalean Fungi from the Ordovician. Science (80-. ). 289: 1920–1921 Available at: https://www.sciencemag.org/lookup/doi/10.1126/science.289.5486.1920 Redkar A, Gimenez Ibanez S, Sabale M, Zechmann B, Solano R & Di Pietro A (2022a) Marchantia polymorpha model reveals conserved infection mechanisms in the vascular wilt fungal pathogen Fusarium oxysporum. New Phytol. 234: 227–241 Redkar A, Sabale M, Schudoma C, Zechmann B, Gupta YK, López-Berges MS, Venturini G, Gimenez-Ibanez S, Turrà D, Solano R & Di Pietro A (2022b) Conserved secreted effectors contribute to endophytic growth and multihost plant compatibility in a vascular wilt fungus. Plant Cell 34: 3214–3232 Rellán-Álvarez R, Lobet G & Dinneny JR (2016) Environmental Control of Root System Biology. Annu. Rev. Plant Biol. 67: 619–642 Remy W, Taylor TN, Hass H & Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci U S A 91: 11841–11843 Available at: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC45331/ [Accessed March 12, 2017] Retallack GJ (1992) Chapter 21 - Paleozoic paleosols. In Weathering, Soils & Paleosols, Martini IP & Chesworth WBT-D in ESP (eds) pp 543–564. Elsevier Available at: https://www.sciencedirect.com/science/article/pii/B978044489198350026X Rich MK, Vigneron N, Liboure C, Keller J, Xue L, Hajheidari M, Radhakrishnan G V., Le Ru A, Diop SI, Potente G, Conti E, Duijsings D, Batut A, Le Faouder P, Kodama K, Kyozuka J, Sallet E, Bécard G, Rodriguez-Franco M, Ott T, et al (2021) Lipid exchanges drove the evolution of mutualism during plant terrestrialization. Science (80-. ). 372: 864–868 Rico-Reséndiz F, Cervantes-Pérez SA, Espinal-Centeno A, Dipp-Álvarez M, Oropeza-Aburto A, Hurtado-Bautista E, Cruz-Hernández A, Bowman JL, Ishizaki K, Arteaga-Vázquez MA, Herrera-Estrella L & Cruz-Ramírez A (2020) Transcriptional and morphophysiological responses of Marchantia polymorpha upon phosphate starvation. Int. J. Mol. Sci. 21: 1–25 Rohart F, Gautier B, Singh A & Lê Cao KA (2017) mixOmics: An R package for ‘omics feature selection and multiple data integration. PLoS Comput. Biol. 13: 1–19 Ross A, Yamada K, Hiruma K, Yamashita-Yamada M, Lu X, Takano Y, Tsuda K & Saijo Y (2014) The Arabidopsis PEPR pathway couples local and systemic plant immunity. EMBO J. 33: 62–75 Rouached H, Arpat AB & Poirier Y (2010) Regulation of phosphate starvation responses in plants: Signaling players and cross-talks. Mol. Plant 3: 288–299 Available at: http://dx.doi.org/10.1093/mp/ssp120 Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A, Holton N, Malinovsky FG, Tör M, de Vries S & Zipfel C (2011) The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23: 2440–2455 Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A & Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 15: 2122–2133 Rush TA, Puech-Pagès V, Bascaules A, Jargeat P, Maillet F, Haouy A, Maës AQM, Carriel CC, Khokhani D, Keller-Pearson M, Tannous J, Cope KR, Garcia K, Maeda J, Johnson C, Kleven B, Choudhury QJ, Labbé J, Swift C, O’Malley MA, et al (2020) Lipochitooligosaccharides as regulatory signals of fungal growth and development. Nat. Commun. 11: Available at: http://dx.doi.org/10.1038/s41467-020-17615-5 Schwessinger B, Roux M, Kadota Y, Ntoukakis V, Sklenar J, Jones A & Zipfel C (2011) Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet. 7: e1002046 Available at: http://dx.plos.org/10.1371/journal.pgen.1002046 [Accessed January 21, 2019] Singh A, Sharma A, Singh N & Nandi AK (2022) MTO1-RESPONDING DOWN 1 (MRD1) is a transcriptional target of OZF1 for promoting salicylic acid-mediated defense in Arabidopsis. Plant Cell Rep. 41: 1319–1328 Available at: https://doi.org/10.1007/s00299-022-02861-2 Somssich M, Khan GA & Persson S (2016) Cell Wall Heterogeneity in Root Development of Arabidopsis. Front. Plant Sci. 7: 1242 Available at: http://journal.frontiersin.org/Article/10.3389/fpls.2016.01242/abstract [Accessed November 24, 2017] Sønderby IE, Burow M, Rowe HC, Kliebenstein DJ & Halkier BA (2010) A complex interplay of three R2R3 MYB transcription factors determines the profile of aliphatic glucosinolates in Arabidopsis. Plant Physiol. 153: 348–363 Sun J, Miller JB, Granqvist E, Wiley-Kalil A, Gobbato E, Maillet F, Cottaz S, Samain E, Venkateshwaran M, Fort S, Morris RJ, Ané JM, Dénarié J & Oldroyd GED (2015) Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell 27: 823–838 Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, dit Frey N, Gianinazzi-Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, et al (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci U S A 110: 20117–20122 Available at: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3864322/ [Accessed March 12, 2017] Touw AJ, Verdecia Mogena A, Maedicke A, Sontowski R, van Dam NM & Tsunoda T (2020) Both Biosynthesis and Transport Are Involved in Glucosinolate Accumulation During Root-Herbivory in Brassica rapa. Front. Plant Sci. 10: 1–13 Tsuda K, Sato M, Stoddard T, Glazebrook J & Katagiri F (2009) Network properties of robust immunity in plants. PLoS Genet. 5: e1000772 Available at: https://dx.plos.org/10.1371/journal.pgen.1000772 [Accessed February 25, 2019] Tsuji J, Jackson EP, Gage DA, Hammerschmidt R & Somerville SC (1992) Phytoalexin accumulation in arabidopsis thaliana during the hypersensitive reaction to Pseudomonas syringae pv syringae. Plant Physiol. 98: 1304–1309 Val-Torregrosa B, Bundó M, Chiou T-J, Flors V & Segundo BS (2021) NITROGEN LIMITATION ADAPTATION functions as a negative regulator of Arabidopsis immunity. Available at: https://doi.org/10.1101/2021.12.09.471910 Wang B, Li K, Wu G, Xu Z, Hou R, Guo B, Zhao Y & Liu F (2022) Sulforaphane, a secondary metabolite in crucifers, inhibits the oxidative stress adaptation and virulence of Xanthomonas by directly targeting OxyR. Mol. Plant Pathol. 23: 1508–1523 Wang W, Yang J, Zhang J, Liu YX, Tian C, Qu B, Gao C, Xin P, Cheng S, Zhang W, Miao P, Li L, Zhang X, Chu J, Zuo J, Li J, Bai Y, Lei X & Zhou JM (2020) An Arabidopsis Secondary Metabolite Directly Targets Expression of the Bacterial Type III Secretion System to Inhibit Bacterial Virulence. Cell Host Microbe 27: 601–613.e7 Available at: https://doi.org/10.1016/j.chom.2020.03.004 Wilson MH, Holman TJ, Sørensen I, Cancho-Sanchez E, Wells DM, Swarup R, Knox JP, Willats WGT, Ubeda-Tomás S, Holdsworth M, Bennett MJ, Vissenberg K & Hodgman TC (2015) Multi-omics analysis identifies genes mediating the extension of cell walls in the Arabidopsis thaliana root elongation zone. Front. Cell Dev. Biol. 3: 1–12 Wittstock U & Burow M (2010) Glucosinolate Breakdown in Arabidopsis: Mechanism, Regulation and Biological Significance. Arab. B. 8: e0134 Wittstock U & Gershenzon J (2002) Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr. Opin. Plant Biol. 5: 300–307 Wolinska KW, Vannier N, Thiergart T, Pickel B, Gremmen S, Piasecka A, Piślewska- Bednarek M, Nakano RT, Belkhadir Y, Bednarek P & Hacquard S (2021) Tryptophan metabolism and bacterial commensals prevent fungal dysbiosis in Arabidopsis roots. Proc. Natl. Acad. Sci. U. S. A. 118: Yamada K, Yamashita‐Yamada M, Hirase T, Fujiwara T, Tsuda K, Hiruma K & Saijo Y (2016) Danger peptide receptor signaling in plants ensures basal immunity upon pathogen‐induced depletion of BAK 1 . EMBO J. 35: 46–61 Yamaguchi Y, Huffaker A, Bryan AC, Tax FE & Ryan CA (2010) PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22: 508–22 Available at: http://www.ncbi.nlm.nih.gov/pubmed/20179141 [Accessed February 19, 2019] Yu P, He X, Baer M, Beirinckx S, Tian T, Moya YAT, Zhang X, Deichmann M, Frey FP, Bresgen V, Li C, Razavi BS, Schaaf G, von Wirén N, Su Z, Bucher M, Tsuda K, Goormachtig S, Chen X & Hochholdinger F (2021) Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation. Nat. Plants 7: 481–499 Available at: http://dx.doi.org/10.1038/s41477-021-00897-y Zhang B, Wang M, Sun Y, Zhao P, Liu C, Qing K, Hu X, Zhong Z, Cheng J, Wang H, Peng Y, Shi J, Zhuang L, Du S, He M, Wu H, Liu M, Chen S, Wang H, Chen X, et al (2021) Glycine max NNL1 restricts symbiotic compatibility with widely distributed bradyrhizobia via root hair infection. Nat. Plants 7: 73–86 Zhang Y & Li X (2019) Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr. Opin. Plant Biol. 50: 29–36 Available at: https://doi.org/10.1016/j.pbi.2019.02.004 Zhao Y, Hull AK, Gupta NR, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J & Celenza JL (2002) Trp-dependent auxin biosynthesis in Arabidopsis: Involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev. 16: 3100–3112 Zhou F, Emonet A, Dénervaud Tendon V, Marhavy P, Wu D, Lahaye T & Geldner N (2020) Co-incidence of Damage and Microbial Patterns Controls Localized Immune Responses in Roots. Cell 180: 440–453.e18 Available at: https://linkinghub.elsevier.com/retrieve/pii/S009286742030060X Zhou Y, Zhou B, Pache L, Chang M, Khodabakhshi AH, Tanaseichuk O, Benner C & Chanda SK (2019a) Metascape provides a biologist-oriented resource for the analysis of systemslevel datasets. Nat. Commun. 10: Available at: http://dx.doi.org/10.1038/s41467-019- 09234-6 Zhou Z, Zhao Y, Bi G, Liang X & Zhou JM (2019b) Early signalling mechanisms underlying receptor kinase-mediated immunity in plants. Philos. Trans. R. Soc. B Biol. Sci. 374: Zhu A, Ibrahim JG & Love MI (2019) Heavy-Tailed prior distributions for sequence count data: Removing the noise and preserving large differences. Bioinformatics 35: 2084– 2092 Zipfel C & Oldroyd GED (2017) Plant signalling in symbiosis and immunity. Nature 543: 328–336 Available at: http://www.nature.com/articles/nature22009 [Accessed February 27, 2019] Zönnchen J, Gantner J, Lapin D, Barthel K, Eschen‐Lippold L, Erickson JL, Landeo Villanueva S, Zantop S, Kretschmer C, Joosten MHAJ, Parker JE, Guerois R & Stuttmann J (2022) EDS1 complexes are not required for PRR responses and execute TNL‐ETI from the nucleus in Nicotiana benthamiana . New Phytol.: 2249–2264
Refereed:	Yes
URI:	http://kups.ub.uni-koeln.de/id/eprint/65573