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Professor Silke Robatzek

Group Leader
Silke Robatzek Group

A paradigm for more than a decade, it has been known that host membranes respond to pathogen perception. It is now clear that the secretory and endocytic trafficking network are engaged by the plant’s immune system to actively defend against potential pathogens. Reciprocally, invasive pathogens have evolved means to utilize these trafficking pathways for the suppression of plant defences and to promote microbial proliferation.

I am particularly interested to understand how host membranes and their cargoes such as the flagellin receptor FLS2 and other pattern recognition receptors (PRRs) are transported through the cell: how this is regulated, how this contributes to PRR abundance control and thus how it regulates defence activation, for example at the level of pathogen-regulated stomatal movements.

“If we are to understand plant-microbe interactions, we need to investigate the associated sub-cellular adaptations at the molecular level.”

To drive our research, we develop methods for quantitative, high-throughput live cell imaging and combine them with genetic and biochemical approaches.

Publications

Meteignier LV, Zhou J, Cohen M, Bhattacharjee S, Brosseau C, Caamal Chan MG, Robatzek S, Moffett P (2016)

NB-LRR signaling induces translational repression of viral transcripts and the formation of RNA processing bodies through mechanisms differing from those activated by UV stress and RNAi. J. Exp. Bot. (2016) doi: 10.1093/jxb/erw042

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Petre B, Kopischke M, Evrard A, Robatzek S, Kamoun S (2016)

Cell re-entry assays do not support models of pathogen-independent translocation of AvrM and AVR3a effectors into plant cells. bioRxiv preprint January 29, 2016 doi: http://dx.doi.org/10.1101/038232

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Abd-El-Haliem A, Vossen JH, van Zeijl A, Dezhsetan S, Testerink C, Seidl MF, Beck M, Strutt J, Robatzek S, Joosten MHAJ (2016)

Biochemical characterization of the tomato phosphatidylinositol-specific phospholipase C (PI-PLC) family and its role in plant immunity. Biochimica et Biophysica Acta (BBA) – Molecular and Cell Biology of Lipids doi:10.1016/j.bbalip.2016.01.017

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Mithoe SC, Ludwig C, Pel MJC, Cucinotta M, Casartelli A, Mbengue M, Sklenar J, Derbyshire P, Robatzek S, Pieterse CMJ, Aebersold R, Menke FLH (2015)

Attenuation of pattern recognition receptor signaling is mediated by a MAP kinase kinase kinase. EMBO reports (2016). DOI 10.15252/embr.201540806

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Postma J, Liebrand TW, Bi G, Evrard A, Bye RR, Mbengue M, Kuhn H, Joosten MH, Robatzek S (2015)

Avr4 promotes Cf-4 receptor-like protein association with the BAK1/SERK3 receptor-like kinase to initiate receptor endocytosis and plant immunity. New Phytol. 2016 Jan 14. doi: 10.1111/nph.13802.

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Giannakopoulou A, Steele JF, Segretin ME, Bozkurt T, Zhou J, Robatzek S, Banfield MJ, Pais M, Kamoun S (2015)

Tomato I2 immune receptor can be engineered to confer partial resistance to the oomycete Phytophthora infestans in addition to the fungus Fusarium oxysporum. Mol Plant Microbe Interact. 2015 Sep 14.

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Frescatada-Rosa M, Robatzek S, Kuhn H (2015)

Should I stay or should I go? Traffic control for plant pattern recognition receptors. Curr Opin Plant Biol: 28: 23-29. doi: 10.1016/j.pbi.2015.08.007.

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Ben Khaled S, Postma J, Robatzek S (2015)

A Moving View: Subcellular Trafficking Processes in Pattern Recognition Receptor-Triggered Plant Immunity. Annu Rev Phytopathol. 201; 53:379-402. doi: 10.1146/annurev-phyto-080614-120347.

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Lee D, Bourdais G, Yu G, Robatzek S, Coaker G (2015)

Phosphorylation of the Plant Immune Regulator RPM1-INTERACTING PROTEIN4 Enhances Plant Plasma Membrane H+-ATPase Activity and Inhibits Flagellin-Triggered Immune Responses in Arabidopsis. Plant Cell. 2015 Jul 21. pii: tpc.114.132308.

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Bourdais G, Burdiak P, Gauthier A, Nitsch L, Salojärvi J, Rayapuram C, Idänheimo N, Hunter K, Kimura S, Merilo E, Vaattovaara A, Oracz K, Kaufholdt D, Pallon A, Anggoro DT, Glów D, Lowe J, Zhou J, Mohammadi O, Puukko T, Albert A, Lang H, Ernst D, Kollist H, Brosché M, Durner J, Borst JW, Collinge DB, Karpiński S, Lyngkjær MF, Robatzek S, Wrzaczek M, Kangasjärvi J, on behalf of the CRK Consortium (2015)

Large-Scale Phenomics Identifies Primary and Fine-Tuning Roles for CRKs in Responses Related to Oxidative Stress. PLoS Genet. 11(7):e1005373. doi: 10.1371/journal.pgen.1005373.

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Patron NJ, Orzaez D, Marillonnet S, Warzecha H, Matthewman C, Youles M, Raitskin O, Leveau A, Farré G, Rogers C, Smith A, Hibberd J, Webb AAR, Locke J, Schornack S, Ajioka J, Baulcombe DC, Zipfel C, Kamoun S, Jones JDG, Kuhn H, Robatzek S, Van Esse HP, Sanders D, Oldroyd G, Martin C, Field R, O'Connor S, Fox S, Wulff B, Miller B, Breakspear A, Radhakrishnan G, Delaux PM, Loqué D, Granell A, Tissier A, Shih P, Brutnell TP, Quick WP, Rischer H, Fraser PD, Aharoni A, Raines C, South PF, Ané JM, Hamberger BR, Langdale J, Stougaard J, Bouwmeester H, Udvardi M, Murray JAH, Ntoukakis V, Schäfer P, Denby K, Edwards KJ, Osbourn A, Haseloff J (2015)

Standards for plant synthetic biology: a common syntax for exchange of DNA parts. New Phytologist 14 Jul 2015 doi: 10.1111/nph.13532

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Postma J, Liebrand TWH, Bi G, Evrard A, Bye RR, Mbengue M, Joosten MHAJ, Silke Robatzek S (2015)

The Cf-4 receptor-like protein associates with the BAK1 receptor-like kinase to initiate receptor endocytosis and plant immunity. bioRxiv preprint May 19, 2015; doi: http://dx.doi.org/10.1101/019471

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Bi G, Liebrand TW, Bye RR, Postma J, van der Burgh AM, Robatzek S, Xu X, Joosten MH (2015)

SOBIR1 requires the GxxxG dimerization motif in its transmembrane domain to form constitutive complexes with receptor-like proteins. Mol Plant Pathol. 2015 Apr 16. doi: 10.1111/mpp.12266.

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Heard W, Sklenar J, Tome DF, Robatzek S, Jones AM (2015)

Identification of regulatory and cargo proteins of endosomal and secretory pathways in Arabidopsis thaliana by proteomic dissection. Mol Cell Proteomics. 2015 Apr 21.

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Du J, Verzaux E, Chaparro-Garcia A, Bijsterbosch G, Keizer LCP, Zhou J, Liebrand TWH, Xie C, Govers F, Robatzek S, van der Vossen EAG, Jacobsen E, Visser RGF, Kamoun S, Vleeshouwers VGAA (2015)

Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nature Plants 1, Article number: 15034 (2015) ​doi:10.1038/nplants.2015.34

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Lozano-Durán R, Robatzek S (2015)

14-3-3 proteins in plant-pathogen interactions. Mol Plant Microbe Interact. 2015 Jan 13. [Epub ahead of print]

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Caillaud MC, Wirthmueller L, Sklenar J, Findlay K, Piquerez SJ, Jones AM, Robatzek S, Jones JD, Faulkner C (2014)

The Plasmodesmal Protein PDLP1 Localises to Haustoria-Associated Membranes during Downy Mildew Infection and Regulates Callose Deposition. PLoS Pathog. 2014 Nov 13;10(11):e1004496. doi: 10.1371/journal.ppat.1004496.

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Beck M, Wyrsch I, Strutt J, Wimalasekera R, Webb A, Boller T, Robatzek S (2014)

Expression patterns of FLAGELLIN SENSING 2 map to bacterial entry sites in plant shoots and roots. J. Exp. Bot. (2014) doi: 10.1093/jxb/eru366

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McLachlan D, Kopischke M and Robatzek S (2014)

Gate control: guard cell regulation by pathogen stress. New Phytol. Volume 203, Issue 4, pages 1049–1063.

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Robatzek, S. (2014)

Endocytosis: At the crossroads of pattern recognition immune receptors and pathogen effectors. Applied Plant Cell Biol: Cellular Tools and Approaches for Plant Biotechnology. Springer. In press. (book chapter)

Beck, M., Zhou, J., Faulkner, C., and Robatzek, S. (2014)

High-throughput imaging of plant immune responses. Methods Mol Biol: Plant Pathogen Interact. Springer. 127:67-80.

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Lozano-Durán, R., Bourdais, G., He, S.Y. and Robatzek, S. (2014)

The bacterial effector HopM1 suppresses stomatal immunity to promote virulence. New Phytologist. 202: 259-269.

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Robatzek, S. (2014)

Illuminating traffic control for cell division planes. eLife 3:e02747 (insight article).

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Spallek, T., Beck, M., Ben Khaled, S., Salomon, S., Bourdais, G., Schellmann, S. and Robatzek, S. (2013)

Sorting by the ESCRT machinery is required for FLS2 endosomal trafficking and plant immunity. PLoS Gen. 9: e1004035.

Bartels, S., Lori, M., Mbengue, M., van Verk, M., Klauser. D., Hander, T., Böni, R., Robatzek, S. and Boller, T. (2013)

The family of AtPeps and their precursors in Arabidopsis: Differential expression and localization but similar induction of pattern-triggered immune responses. J Exp. Bot. 64: 5309-5321.

Liebrand, T.W., Kombrink, A., Zhang, Z., Sklenar, J., Jones, A.M., Robatzek, S., Thomma, B.P. and Joosten, M.H. (2013)

Chaperones of the endoplasmic reticulum are required for Ve1-mediated resistance to Verticillium. Mol Plant Pathol. 15: 109-117.

Sawinski, K., Mersmann, S., Robatzek, S. and Böhmer, M. (2013)

Guarding the green: Pathways to stomatal immunity. Mol. Plant Microbe Interact. 26: 626-632. (review)

Liebrand, T.W.H. van den Berg, G.C.M., Zhang, Z., Smit, P., Cordewener, J.H.G., America, A.H.P., Sklenar, J., Jones, A.M.E., Tameling, W.I.L., Robatzek, S., Thomma, B.P.H.J. and Joosten, M.H.A.J. (2013)

The receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc. Natl. Acad. Sci. USA. 110: 10010-10015.

Faulkner C., Petuschnig, E., Benitz-Alfonso, Y., Beck, M., Robatzek, S., Lipka, V. and Maule A.J. (2013)

LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc. Natl. Acad. Sci. USA. 110: 9166-9170.

Du, Y., Tejos, R., Beck, M., Himschoot, E., Li, H., Robatzek, S., Vanneste, S., Friml, J. (2013)

Salicylic acid interferes with clathrin-mediated, Brefeldin A-sensitive endocytic protein trafficking. Proc. Natl. Acad. Sci. USA. 110:7946-7951.

Fitzgibbon, J., Beck, M., Zhou, J., Faulkner, C., Robatzek, S. and Oparka, K. (2013)

A developmental framework for complex plasmodesmata formation revealed by large-scale imaging of the Arabidopsis leaf epidermis. Plant Cell. 25: 57-70.

Zhou, J., Spallek, T., Faulkner, C. and Robatzek, S. (2012)

CalloseMeasurer: A Novel Software Solution to Measure Callose Deposition and Recognise Spreading Callose Patterns. Plant Methods. 2012. 8: 49.

Win, J., Chaparro-Garcia, A., Belhaj, K., Saunders, D.G.O., Yoshida, K., Dong, S., Schornack, S., Zipfel, C., Robatzek, S., Hogenhout, S.A., and Kamoun, S. 2012.

Effector Biology of Plant-associated Organisms: Concepts and Perspectives. Cold Spring Harbor Symposium on Quantitative Biology, 77:235-247.

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Beck, M., Zhou, J., Faulkner, C., MacLean, D. and Robatzek, S. (2012)

Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. Plant Cell. 24: 4205-4219.

Robatzek, S. and Wirthmueller, L. (2012)

Mapping FLS2 function to structure: LRRs, kinase and its working bits. Protoplasma. 250: 671-681. (review)

Faulkner, C. and Robatzek, S. (2012)

Plants and pathogens: putting infection strategies and defence mechanisms on the map. Curr Opin Plant Biol. 77: 235-247. (review)

Beck, M., Heard, W., Mbengue, M. and Robatzek, S. (2012)

The INs and OUTs of pattern recognition receptors at the cell surface. Curr Opin Plant Biol. 15: 367-374. (review)

Segonzac C, Nimchuk ZL, Beck M, Robatzek S, Meyerowitz EM and Zipfel C (2012)

The shoot apical meristem regulatory peptide CLV3 does not activate innate immunity. Plant Cell, 24(8): 3186-3192.

Göhre, V., Jones, A.M.E., Sklenář, J., Robatzek, S. and Weber, A.P.M. (2012)

Crosstalk between PAMP-triggered immunity and photosynthesis. Mol. Plant Microbe Interact. 25: 1083-1092.

Liebrand, T.W., Smit, P., Abd-El-Haliem, A., de Jonge, R., Cordewener, J.H., America, A.H., Sklenar, J., Jones, A.M., Robatzek, S., Thomma, B.P., Tameling, W.I. and Joosten, M.H. (2012)

ER-Quality Control Chaperones Facilitate the Biogenesis of Cf Receptor-Like Proteins Involved in Pathogen Resistance of Tomato. Plant Physiol. 159: 1819-1833.

Frei dit Frey, N., Mbengue, M., Kwaaitaal, M., Nitsch, L., Altenbach, D., Häweker, H., Lozano-Duran, R., Njo, M.F., Beeckman, T., Huettel, B., Borst, J.W., Panstruga, R. and Robatzek, S. (2012)

Plasma membrane calcium ATPases are important components of receptor-mediated signalling in plant immune responses and development. Plant Physiol. 159: 798-809.

Lu, Y.-J., Schornack, S., Spallek, T., Geldner, N., Chory, J., Schellmann, S., Schumacher, K., Kamoun, S., and Robatzek, S. 2012.

Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cellular Microbiology, 14:682-697

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Vetter, M.M., He, F., Kronholm, I., Häweker, H., Reymond, M., Bergelson, J., Robatzek, S. and de Meaux, J. (2012)

Flagellin perception varies quantitatively in Arabidopsis thaliana and its relatives. Mol. Biol. Evol. 29: 1655-1667.

Beck, M. and Robatzek, S. (2011)

Receptor trafficking in plants. Signaling and Communication in Plants: Receptor-like Kinases in Plants. Springer. 13: 253-274.

Oldroyd, G.E. and Robatzek, S. (2011)

The broad spectrum of plant associations with other organisms. Curr. Opin. Plant Biol. 14: 347-350.

Keinath, N.F., Kierszniowska, S., Lorek, J., Bourdais, G., Kessler, S.A., Asano, H., Grossniklaus, U., Schulze, W., Robatzek, S. and Panstruga, R. (2010)

PAMP-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J. Biol. Chem. 285: 39140-39149.

Salomon, S., Grunewald, D., Stüber, K., Schaaf, S., MacLean, D., Schulze-Lefert, P. and Robatzek, S. (2010)

High throughput confocal imaging of intact live tissue enables quantification of membrane trafficking in Arabidopsis. Plant Physiol. 154: 1096-1104.

Zipfel, C. and Robatzek, S.

PAMP-triggered immunity: veni, vidi, …? Plant Physiol. 154: 551-554. (review)

Mersmann, S., Bourdais, G., Rietz, S. and Robatzek, S.

Ethylene signalling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiol. 154: 391-400.

Malinovsky FG, Brodersen P, Fiil BK, McKinney LV, Thorgrimsen S, Beck M, Nielsen HB, Pietra S, Zipfel C, Robatzek S, Petersen M, Hofius D, and Mundy J (2010)

Lazarus1, a DUF300 protein, contributes to programmed cell death associated with Arabidopsis acd11 and the hypersensitive response. PLoS One, 5(9). pii: e12586.

Paungfoo-Lonhienne, C., Rentsch, D., Robatzek, S., Webb, R.I., Sagulenko, E., Näsholm, T., Schmidt, S., Lonhienne, T.G.

Turning the table: plants consume microbes as a source of nutrients. PLoS One 5:e11915.

Wrzaczek, M., Brosche, M., Salojarvi, J., Kangasjarvi, S., Idanheimo, N., Mersmann, S., Robatzek, S., Karpinski, S., Karpinska, B. and Kangasjarvi, J.

Transcriptional regulation of the CRK/DUF26 group of Receptor-like protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biol. 10: 95.

Häweker, H., Ripps, S., Koiwa, H., Salomon, S., Saijo, Y., Chinchilla, D., Robatzek, S. and von Schaewen, A. (2010)

Pattern recognition receptors require N-glycosylation to mediate plant immunity. Journal Biol. Chem. 285: 4629-4636.

Saijo Y, Tintor N, Lu X, Rauf P, Pajerowska-Mukhtar K, Häweker H, Dong X, Robatzek S, Schulze-Lefert P. (2009)

Receptor quality control in the endoplasmic reticulum for plant innate immunity. EMBO J. 4;28(21):3439-49

Göhre V, Spallek T, Häweker H, Mersmann S, Mentzel T, Boller T, de Torres M, Mansfield JW, Robatzek S. (2008)

Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol. 2008 Dec 9;18(23):1824-32.

Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G and Boller T (2007)

A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature, 448: 497-500.

Felix G, Bittel P, Chinchilla D, Kunze G, Robatzek S, Zipfel C and Boller T (2006)

Receptor-like kinases and innate immunity in plants. In: Sanchez F., Geiger O. (ed). International Society for Molecular Plant-Microbe Interactions, St. Paul, Minnesota. Biology of Plant-Microbe Interactions, 5: 21-29.

Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T and Felix G (2004)

The N-terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell, 16 (12): 3496-3507.

Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T and Jones JDG (2004)

The transcriptional innate immune responses to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiology, 135: 1113-1128.

Zipfel C, Robatzek S, Navarro L, Oakeley E, Jones JDG, Felix G and Boller T (2004).

Bacterial disease resistance through flagellin perception in Arabidopsis. Nature, 428: 764-767.

Navarro L, Zipfel C, Rowland O, Robatzek S, Boller T and Jones JDG (2003)

mRNA expression profiling of the Arabidopsis flg22-triggered innate immune response and the Avr9/Cf-9 response in tobacco. In: Tikhonovich I, Lugtenberg B, and Provorov N (ed). International Society for Molecular Plant-Microbe Interactions, St. Paul, Minnesota. Biology of Plant-Microbe Interactions, 4: 237-239.

Job History

2009 – present Group Leader, The Sainsbury Laboratory

2009 – present Honorary Professor (Habilitation in Cell Biology 2009), Botanical Institute, University of Basel, Switzerland

2005 – 2009 Group Leader,

2001 – 2005 Postdoctoral Fellow, Friedrich-Miescher Institute for Biomedical Research & Botanical Institute, University of Basel, Switzerland

2000 – 2001 Postdoctoral Fellow, Max-Planck-Institute for Plant Breeding Research, Cologne, Germany

1997 – 2000 PhD Student (PhD in Biochemistry 2000), Max-Planck-Institute for Plant Breeding Research, Cologne, Germany

1991 – 1997 Undergraduate Student (Diploma in Biology 1997), University of Göttingen, Germany