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Institute for Plant SciencesAG Zuccaro

Publications

2023

Eichfeld R, Mahdi LK, De Quattro C, Armbruster L, Endeshaw AB, Miyauchi S, Hellmann MJ, Cord-Landwehr S, Grigoriev I, Peterson D, Singan V, Lail K, Savage E, Ng V, Langen G, Moerschbacher BM, Zuccaro A (2023) Time-resolved transcriptomics reveal a mechanism of host niche defense: beneficial root endophytes deploy a host-protective antimicrobial GH18-CBM5 chitinase. BioRxiv doi: 10.1101/2023.12.29.572992

Llamas E, Koyuncu S, Lee HJ, Wehrmann M, Gutierrez-Garcia R, Dunken N, Charura N, Torres-Montilla S, Schlimgen E, Mandel AM, Theile EB, Grossbach J, Wagle P, Lackmann JW, Schermer B, Benzing T, Beyer A, Pulido P, Rodriguez-Concepcion M, Zuccaro A & Vilchez D (2023) In planta expression of human polyQ-expanded huntingtin fragment reveals mechanisms to prevent disease-related protein aggregation. Nature Aging doi: 10.1038/s43587-023-00502-1

Zecua-Ramirez P, Llamas E, Charura N, Dunken N, De Quattro C, Mandel A, Langen G, Dagdas Y, Zuccaro A (2023) Autophagy restricts fungal accommodation in the roots of Arabidopsis thaliana. BioRxiv doi: 10.1101/2023.07.21.550010

Kelly S, Hansen SB, Rübsam H, Saake P, Pedersen EM, Gysel K, Madland E, Wu S, Wawra S, Reid D, Sullivan JT, Blahovska Z, Vinther M, Muszynski A, Azadi P, Thygesen MB, Aachmann FL, Ronson CW, Zuccaro A, Andersen KR, Radutoiu S, Stougaard J (2023) A glycan receptor kinase facilitates intracellular accommodation of arbuscular mycorrhiza and symbiotic rhizobia in the legume Lotus japonicus. PLOS Biology doi: 10.1371/journal.pbio.3002127

Wanke A, van Boerdonk S, Mahdi LK, Wawra S, Neidert M, Chandrasekar B, Saake P, Saur IML, Derbyshire P, Holton N, Menke FLH, Brands M, Pauly M, Acosta IF, Zipfel C, Zuccaro A (2023) A GH81-type ß-glucan-binding protein enhances colonization by mutualistic fungi in barley. Current Biology doi: 10.1016/j.cub.2023.10.048

Charura N, Llamas E, De Quattro C, Vilchez D, Nowack MK, Zuccaro A (2023) Root cap cell corpse clearance limits microbial colonization in Arabidopsis thaliana. BioRxiv doi: 10.1101/2023.02.03.526420

2022

Dunken N, Mahdi L, Häusler RE, Zuccaro A (2022) Monitoring Cell Death Via Ion Leakage and PAM Fluorometry. In: Klemenčič M, Stael S, Huesgen PF (eds) Plant Proteases and Plant Cell Death. Methods in Molecular Biology, vol 2447. Humana, New York, NY doi: 10.1007/978-1-0716-2079-3_14

Redkar A, Sabale M, Zuccaro A, Di Pietro A (2022) Determinants of endophytic and pathogenic lifestyle in root colonizing fungi. Current Opinion in Plant Biology doi:10.1016/j.pbi.2022.102226

Llamas E, Koyuncu S, Lee HJ, Gutierrez-Garcia R, Dunken N, Charura N, Torres-Montilla S, Schlimgen E, Pulido P, Rodriguez-Concepcion M, Zuccaro A, Vilchez D (2022) Chloroplast protein import determines plant proteostasis and retrograde signaling. BioRxiv doi: 10.1101/2022.03.19.484971

Dunken N, Widmer H, Balcke GU, Straube H, Langen G, Charura NM, Saake P, Leson L, Roevenich H, Wawra S, Djamei A, Tissier AF, Witte CPF, Zuccaro A (2022) A fungal endophyte-generated nucleoside signal regulates host cell death and promotes root colonization. BioRxiv doi: 10.1101/2022.03.11.483938

Chandrasekar B, Wanke A, Wawra S, Saake P, Mahdi LK, Charura N, Neidert M, Poschmann G, Malisic M, Thiele M, Stühler K, Dama M, Pauly M, Zuccaro A (2022) Fungi hijack a ubiquitous plant apoplastic endoglucanase to release a ROS scavenging β-glucan decasaccharide to subvert immune responses. The Plant Cell doi: 10.1093/plcell/koac114

Mahdi LK, Miyauchi S, Uhlmann C, Garrido-Oter R, Langen G, Wawra S, Niu Y, Robertson-Albertyn S, Bulgarelli D, Parker JE, Zuccaro A (2021) The fungal root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with the microbiota in Arabidopsis thaliana and barley. ISME Journal doi: 10.1038/s41396-021-01138-y

Vanacore A, Vitiello G, Wanke A, Cavasso D, Clifton L, Mahdi L, Campanero-Rhodes MA, Solís D, Wuhrer M, Nicolardi S, Molinaro A, Marchetti R, Zuccaro A, Paduano L, Silipo A (2022) Lipopolysaccharide O-antigen molecular and supramolecular modifications of plant root microbiota are pivotal for host recognition. Carbohydrate Polymers doi: 10.1016/j.carbpol.2021.118839

2021

Harris JM, Jones KM, Wang D, Zuccaro A (2021) Focus on How Plants Engage With Beneficial Microorganisms While at the Same Time Restricting Pathogens. MPMI Focus Issue doi: 10.1094/MPMI-03-21-0060-FI

Liu Y, Balcke GU, Porzel A, Mahdi LK, Scherr-Henning A, Bathe U, Zuccaro A, Tissier A (2021) A barley gene cluster for the biosynthesis of diterpenoid phytoalexins. BioRxiv doi: 10.1101/2021.05.21.445084

Llamas E, Torres-Montilla S, Lee HY, Barja MV, Schlimgen E, Dunken N, Wagle P, Werr W, Zuccaro A, Rodríguez-Concepción M, Vilchez D (2021) The intrinsic chaperone network of Arabidopsis stem cells confers protection against proteotoxic stress. Aging Cell doi:10.1111/acel.13446

Wanke A, Malisic M, Wawra S, Zuccaro A (2021) Unraveling the sugar code: the role of microbial extracellular glycans in plant-microbe interactions. Journal of Experimental Botany doi: 10.1093/jxb/eraa414

2020

Dietzen C, Koprivova A, Whitcomb SJ, Langen G, Jobe TO, Hoefgen R, Kopriva S (2020) The Transcription Factor EIL1 Participates in the Regulation of Sulfur-Deficiency Response. Plant Physiology doi: 10.1104/pp.20.01192

Sanchez-Vallet A, Tian H, Rodriguez-Moreno L, Valkenburg DJ, Saleem-Batcha R, Wawra S, Kombrink A, Verhage L, de Jong R, van Esse P, Zuccaro A, Croll D, Mesters J, Thomma BPHJ (2020) A secreted LysM effector protects fungal hyphae through chitin-dependent homodimer polymerization. PLOS Pathogens doi: 10.1371/journal.ppat.1008652

Zuccaro A, Langen G (2020) Breeding for resistance: can we increase crop resistance to pathogens without compromising the ability to accommodate beneficial microbes? New Phytologist doi:10.1111/nph.16610

Nostadt R, Hilbert M, Nizam S, Rovenich H, Wawra S, Martin J, Küpper H, Mijovilovich A, Ursinus A, Langen G, Hartmann MD, Lupas A, Zuccaro A (2020) A secreted fungal histidine- and alanine-rich protein regulates metal ion homeostasis and oxidative stress. New Phytologist doi: 10.1111/nph.16606

Hilbert M, Novero M, Rovenich H, Mari S, Grimm C, Bonfante P, Zuccaro A (2020) MLO differentially regulates barley root colonization by beneficial endophytic and mycorrhizal fungi. Frontiers in Plant Science-Plant Microbe Interactions doi: 10.3389/fpls.2019.01678

Wanke A, Rovenich H, Schwanke F, Velte S, Becker S, Hehemann JH, Wawra S, Zuccaro A (2020) Plant species-specific recognition of long and short ß-1,3- linked glucans is mediated by different receptor systems. The Plant Journal doi: 10.1111/tpj.14688

Zuccaro A (2020) Plant phosphate status drives host microbial preferences: a trade-off between fungi and bacteria (Commentary). EMBO Journal doi: 10.15252/embj.2019104144

2019

Koprivova A, Schuck S, Jacoby R, Klinkhammer I, Welter B, Leson L, Martyn A, Nauen J, Grabenhorst N, Mandelkow JF, Zuccaro A, Zeier J, Kopriva S (2019) Root-specific camalexin biosynthesis controls the plant growth promoting effects of multiple bacterial strains. PNAS doi: 10.1073/pnas.1818604116

Sarkar D, Rovenich H, Jeena G, Nizam S, Tissier A, Balcke GU, Mahdi L, Bonkowski M, Langen G, Zuccaro A (2019) The inconspicuous gatekeeper: endophytic Serendipita vermifera acts as extended plant protection barrier in the rhizosphere. New Phytologist doi: 10.1111/nph.15904

Wawra S, Fesel P, Widmer H, Neumann U, Lahrmann U, Becker S, Hehemann J, Langen G, Zuccaro A  (2019) FGB1 and WSC3 are in planta-induced β-glucan-binding fungal lectins with different functions. New Phytologist doi: 10.111/nph.15711

Nizam S, Qiang X, Wawra S, Nostadt R, Getzke F, Schwanke F, Dreyer I, Langen G, Zuccaro A (2019) Serendipita indica E5'NT modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization. EMBO Reports 20(2). pii: e47430. doi: 10.15252/embr.201847430

2018

Dreyer I, Spitz O, Kanonenberg K, Montag K, Handrich M, Ahmad S, Schott-Verdugo S, Navarro-Retamal C, Rubio-Meléndez M, Gomez-Porras JL, Riedelsberger J, Molina-Montenegro M, Succurro A, Zuccaro A, Gould S, Bauer P, Schmitt L, Gohlke H (2019) Nutrient exchange in arbuscular mycorrhizal symbiosis from a thermodynamic point of view. New Phytologist doi: 10.1111/nph.15646

2017

Almario J, Jeena G, Wunder J, Langen G, Zuccaro A, Coupland G, Bucher M (2017) Root-associated fungal microbiota of non-mycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition. PNAS 114(44):E9403-E9412. doi: 10.1073/pnas.1710455114

2016

Rovenich H, Zuccaro A, Thomma BPHJ (2016) Convergent evolution of filamentous microbes towards evasion of glycan-triggered immunity. New Phytologist 212(4):896-901. doi: 10.1111/nph.14064

Fesel PH, Zuccaro A (2016) Dissecting endophytic lifestyle along the parasitism/mutualism continuum in Arabidopsis. Current Opinion in Microbiology doi: 10.1016/j.mib.2016.05.008

Wawra S, Fesel P, Widmer H, Leson L, Langen G, et al. (2016) The fungal-specific ß-glucan binding lectin FGB1 alters cell wall composition and prevents glucan-triggered immunity in plants. Nature Communications 7, 13188. doi: 10.1038/ncomms13188

Weiß M, Waller F, Zuccaro A, Selosse MA (2016) Sebacinales - one thousand and one interactions with land plants. New Phytologist doi: 10.1111/nph.13977

Fesel PH, Zuccaro A (2016) β-glucan: Crucial component of the fungal cell wall and elusive MAMP in plants. Fungal Genetics and Biology 90, 53-60. doi: 10.1016/j.fgb.2015.12.004

2015

Lo Presti L, Lanver D, Schweizer G, Tanaka S, Liang L, et al. (2015) Fungal Effectors and Plant Susceptibility. Annual Review of Plant Biology, Vol 66. pp. 513-545.

Lahrmann U, Strehmel N, Langen G, Frerigmann H, Leson L, et al. (2015) Mutualistic root endophytism is not associated with the reduction of saprotrophic traits and requires a noncompromised plant innate immunity. New Phytologist 207: 841-857.

Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, et al. (2015) Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nature Genetics 47: 410-U176.

Banhara A, Ding Y, Kuehner R, Zuccaro A, Parniske M (2015) Colonization of root cells and plant growth promotion by Piriformospora indica occurs independently of plant common symbiosis genes. Frontiers in Plant Science 6.

2014

Zuccaro A, Lahrmann U, Langen G (2014) Broad compatibility in fungal root symbioses. Current Opinion in Plant Biology 20: 135-145.

2013

Zuccaro A (2013) Leben im Untergrund: Wurzel-Endophyten als heimliche Helfer. BIOspektrum 19: 220-221.

Oberwinkler F, Riess K, Bauer R, Selosse M-A, Weiß M, et al. (2013) Enigmatic Sebacinales. Mycological Progress 12: 1-27.

Lahrmann U, Ding Y, Banhara A, Rath M, Hajirezaei MR, et al. (2013) Host-related metabolic cues affect colonization strategies of a root endophyte. Proceedings of the National Academy of Sciences of the United States of America 110: 13965-13970.

Hilbert M, Nostadt R, Zuccaro A (2013) Exogenous auxin affects the oxidative burst in barley roots colonized by Piriformospora indica. Plant signaling & behavior 8: e23572.

2012

Lahrmann U, Zuccaro A (2012) Opprimo ergo sum-Evasion and Suppression in the Root Endophytic Fungus Piriformospora indica. Molecular Plant-Microbe Interactions 25: 727-737.

Hilbert M, Voll LM, Ding Y, Hofmann J, Sharma M, et al. (2012) Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots. New Phytologist 196: 520-534.

Basiewicz M, Weiss M, Kogel K-H, Langen G, Zorn H, et al. (2012) Molecular and phenotypic characterization of Sebacina uermifera strains associated with orchids, and the description of Piriformospora williamsii sp nov. Fungal Biology 116: 204-213.

2011

Zuccaro A, Lahrmann U, Gueldener U, Langen G, Pfiffi S, et al. (2011) Endophytic Life Strategies Decoded by Genome and Transcriptome Analyses of the Mutualistic Root Symbiont Piriformospora indica. Plos Pathogens 7.

Schikora A, Schenk ST, Stein E, Molitor A, Zuccaro A, et al. (2011) N-Acyl-Homoserine Lactone Confers Resistance toward Biotrophic and Hemibiotrophic Pathogens via Altered Activation of AtMPK6. Plant Physiology 157: 1407-1418.

2009

Zuccaro A, Basiewicz M, Zurawska M, Biedenkopf D, Kogel K-H (2009) Karyotype analysis, genome organization, and stable genetic transformation of the root colonizing fungus Piriformospora indica. Fungal Genetics and Biology 46: 543-550.

Schoch CL, Sung G-H, Lopez-Giraldez F, Townsend JP, Miadlikowska J, et al. (2009) The Ascomycota Tree of Life: A Phylum-wide Phylogeny Clarifies the Origin and Evolution of Fundamental Reproductive and Ecological Traits. Systematic Biology 58: 224-239.

Jones EBG, Zuccaro A, Mitchell J, Nakagiri A, Chatmala I, et al. (2009) Phylogenetic position of freshwater and marine Sigmoidea species: introducing a marine hyphomycete Halosigmoidea gen. nov (Halosphaeriales). Botanica Marina 52: 349-359.

2008

Zuccaro A, Schoch CL, Spatafora JW, Kohlmeyer J, Draeger S, et al. (2008) Detection and identification of fungi intimately associated with the brown seaweed Fucus serratus. Applied and Environmental Microbiology 74: 931-941.

Zuccaro A, Goetze S, Kneip S, Dersch P, Seibel J (2008) Tailor-made fructooligosaccharides by a combination of substrate and genetic engineering. Chembiochem 9: 143-149.

Sharma M, Schmid M, Rothballer M, Hause G, Zuccaro A, et al. (2008) Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cellular Microbiology 10: 2235-2246.

Proksch P, Ebel R, Edrada R, Riebe F, Liu H, et al. (2008) Sponge-associated fungi and their bioactive compounds: the Suberites case. Botanica Marina 51: 209-218.

Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, et al. (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytologist 180: 501-510.

2007

Roth A, Zuccaro A, Kneip S, Dersch P (2007) Characterization of a new inducible promoter for protein expression in Aspergillus niger, using a green fluorescent protein reporter system. Journal of Biotechnology 131: S256-S257.

2006

Mitchell JI, Zuccaro A (2006) Sequences, the environment and fungi. Mycologist 20: 62-74.

2005

Zuccaro A, Mitchell J (2005) The Fungal Community its Organization And Role In The Ecosystem. The Fungal Community. Boca Raton, FL: Taylor & Francis.

2004

Zuccaro A, Summerbell R, Gams W, Schroers H, Mitchell J (2004) A new Acremonium species associated with Fucus spp., and its affinity with a phylogenetically distinct marine Emericellopsis clade. Studies in Mycology: 283-297.

Sigler L, Zuccaro A, Summerbell R, Mitchell J, Pare J (2004) Acremonium exuviarum sp nov., a lizard-associated fungus with affinity to Emericellopsis. Studies in Mycology: 409-413.

Adolph S, Bach S, Blondel M, Cueff A, Moreau M, et al. (2004) Cytotoxicity of diatom-derived oxylipins in organisms belonging to different phyla. Journal of Experimental Biology 207: 2935-2946.

2003

Zuccaro A, Schulz B, Mitchell J (2003) Molecular detection of ascomycetes associated with Fucus serratus. Mycological Research 107: 1451-1466.

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