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Project 18
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Project 18

Paul Schulze-Lefert

Intracellular perception of fungal effectors and initiation of signalling by allelic NB-LRR receptors

Max-Planck-Institute for Plant Breeding Research, Cologne


Brief description in German:
Wir untersuchen den Wirkmechanismus von MLA Immunrezeptoren der CC-NB-LRR Klasse, die isolat-spezifische Immunantworten gegen den Mehltaupilz in Gerste und Arabidopsis auslösen. MLA Rezeptoren wirken im Kern und sind dort durch Assoziation mit WRKY Transkriptionsfaktoren an der transkriptionellen Umprogrammierung beteiligt. Wir werden die nukleären Wirkorte und die Dynamik der Umprogrammierung durch eine Kombination von genomweiten Transkript- und Chromatinanalysen aufklären. Wir nutzen Proteinstruktur-geführte Funktionsanalysen um den Aktivierungsmechanismus der Rezeptoren besser zu verstehen.

We study the molecular mechanisms underlying isolate-specific immune responses initiated by intracellular CC-NB-LRR type MLA receptors to the powdery mildew fungus in barley and Arabidopsis.

MLA immune sensors act in the nucleus by association with WRKY transcription factors, thereby contributing to the transcriptional reprogramming of plant cells. We will define nuclear action sites of MLA receptors and the dynamics of the reprogramming process through a combination of genome-wide transcript profiling and chromatin studies. Structure-guided functional studies will assist to understand the activation mechanism of these immune sensors.

Like animals, plants have evolved elaborate surveillance systems to protect themselves against infection by pathogenic microorganisms. One surveillance system involves immune receptors, called resistance (R) proteins, which typically detect isolate-specific pathogen effector molecules. Upon recognition of these effectors, R proteins trigger effective immune responses that are usually linked to a rapid cellular suicide of attacked plant cells, designated the hypersensitive response (HR).

Most known intracellular R proteins have a tripartite architecture consisting of N-terminal coiled-coil (CC) or TOLL/Interleukin-1 receptor (TIR) domains, a central nucleotide binding (NB) site, and C-terminal leucine-rich repeats (LRRs). Plant NB-LRR type R proteins structurally resemble mammalian intracellular NOD/NACHT/CATERPILAR proteins that utilize NF-κB for signalling and the apoptotic machinery for execution of innate immune responses. The mode of action of this class of immune sensors in both plants and animals is still largely unknown (or controversial).

Our aim is to unravel the mechanisms underlying isolate-specific immune responses initiated by allelic CC-NB-LRR type MLA receptors to the powdery mildew fungus in barley.

We established that MLA immune sensors act in the nucleus, partly by nuclear associations with WRKY transcriptional repressors, implicating direct associations with the transcriptional machinery and a short signalling pathway.

In collaboration with a structural biology group, we have resolved the crystal structure of the MLA CC domain, providing insight in possible receptor activation mechanisms. Remarkably, race-specific MLA-triggered immunity to the powdery mildew fungus is fully functional in transgenic Arabidopsis, a species that diverged from barley 150 My ago.

Our future goals during the next phase of the CRC 670 include the comprehensive identification of nuclear action sites of MLA receptors through a combination of genome-wide transcript profiling and chromatin studies using next generation sequencing and chromatin-immunoprecipitation technologies (ChIP-Seq). In parallel, we will employ structure-guided functional studies to better understand the activation mechanism of this receptor.

We expect that the proposed comparative analysis of MLA immune functions in barley and Arabidopsis will facilitate the identification of a common principle underlying nuclear MLA activities. Interactions within the CRC 670 have been initiated with the group of I. Somssich (sub-project 24) on transcriptional reprogramming. Our work is complementary with the group of T. Kufer (sub-project N01) working on NOD proteins and synergistic with the group of J. Parker (sub-project 19) focussing on TIR-NB-LRR-triggered nucleo-cytoplasmic signalling.


List of publications resulting from the project

Peer-reviewed publications:

Hacquard S, Kracher B, Maekawa T, Vernaldi S, Schulze-Lefert P, Ver Loren van Themaat E. (2013) Mosaic genome structure of the barley powdery mildew pathogen and conservation of transcriptional programs in divergent hosts. Proc Natl Acad Sci USA. 110(24):E2219-28. doi: 10.1073/pnas.1306807110

Bai S, Liu J, Chang C, Zhang L, Maekawa T, Wang Q, Xiao W, Liu Y, Chai J, Takken FL, Schulze-Lefert P, Shen QH. (2012) Structure-function analysis of barley NLR immune receptor MLA10 reveals its cell compartment specific activity in cell death and disease resistance. PLoS Pathog. 8(6):e1002752. doi: 10.1371/journal.ppat.1002752

Maekawa T, Kracher B, Vernaldi S, Ver Loren van Themaat E, Schulze-Lefert P. (2012) Conservation of NLR-triggered immunity across plant lineages. Proc Natl Acad Sci USA. 109(49):20119-23. doi: 10.1073/pnas.1218059109. Epub 2012 Nov 21.

Maekawa, T., Cheng, W., Spiridon, L.N., Töller, A., Lukasik, E., Saijo, Y., Liu, P., Shen, Q.-H., Micluta, M.A., Somssich, I.E., Takken, F.L.W., Petrescu, A.-J., Chai, J., and Schulze-Lefert P. (2011) Coiled-coil domain-dependent homodemerization of intracellular barley immune receptors defines a minimal functional module for triggering cell death, Cell Host & Microbe 9, 187-199

Humphry, M., Bednarek, P., Kemmerling, B., Koh, S., Stein, M., Göbel, U., Stüber, K., Pislewska-Bednarek, M., Loraine, A., Schulze-Lefert, P., Somerville, S., and Panstruga, R. (2010). A regulon conserved in monocot and dicot plants defines a functional module in antifungal plant immunity, PNAS 107: 21896-21901

Kwon, C., Neu, C., Pajonk, S., Yun, HS., Lipka, U., Humphry, M.E., Bau, S., Straus, M., Rampelt, H., El Kasmi, F., Jürgens, G., Parker, J., Panstruga, R., Lipka, V., and Schulze-Lefert P. (2008). Co-option of a default secretory pathway for plant immune responses, Nature 451, 835-840.

Kwon, C, Panstruga, R., and Schulze-Lefert, P. (2008). Les liaisons dangereuses: immunological synapse formation in animals and plants. Trends in Immunology 29, 159-166.

Pajonk, S., Kwon, C., Clemens, N., Panstruga, R., and Schulze-Lefert P. (2008). Activity determinants and functional specialization of Arabidopsis PEN1 syntaxin in innate immunity. Journal of Biological Chemistry 283, 26974-26984.

Shen, Q.-H., Saijo, Y., Mauch, S., Biskup, C., Bieri, S., Keller, B., Seki, H., Ülker, B., Somssich I.E., and Schulze-Lefert P. (2007). Nuclear Activity of MLA Immune Receptors Links Isolate-Specific and Basal Disease-Resistance Responses. Science 315, 1098-1103.

Shen, Q.-H., and Schulze-Lefert P. (2007). Rumble in the nuclear Jungle: compartmentalization, trafficking, and nuclear action of plant immune receptors. EMBO J. 26, 4239-4301.

Reviews :
Griebel T, Maekawa T, Parker JE.
NOD-like receptor cooperativity in effector-triggered immunity. (2014) Trends Immunol. 35(11):562-570. doi: 10.1016/j.it.2014.09.005. [Epub ahead of print] Review.

Jacob F, Vernaldi S, Maekawa T. (2013) Evolution and Conservation of Plant NLR Functions. Front Immunol. 4:297. doi: 10.3389/fimmu.2013.00297. Review.

Non peer-reviewed publications:
Panstruga, R., Parker, J.E., and Schulze-Lefert, P. (2009). Cell SnapShot: Plant immune response pathways. Cell 135, 978.e1-978.e3.

Yun, HS., Panstruga, R, Schulze-Lefert, P., and Kwon, C. (2008). Ready to fire - secretion in plant immunity. Plant Signaling & Behavior 3, 505-508.

R Functions. Front Immunol. 4:297. doi: 10.3389/fimmu.2013.00297. Review.

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