Laboratory of Biochemistry - Redox Cell Surface Signalling

In multicellular organisms, Reactive Oxygen Species (ROS) are produced in different intra- and extra-cellular compartments in response to a broad spectrum of stresses. ROS control not only the adaptation to stress but also growth and immunity processes. Especially for sessile organisms, like plants, ROS are essential components of multiple signalling pathways for communication between the environment and the interior of the cell. Similarly, to ROS, Receptor Kinases (RKs) also play a crucial role in a broad variety of plant developmental and defence related processes, including pathogen sensing, stem cell maintenance, cell proliferation, cell expansion, stomata development, as well as abiotic stress responses. However, it is still unclear how RKs and ROS signalling networks are linked in the extracellular space.

The main research focus of our group is to understand:

1- How seemingly independent cell surface ROS and RKs signalling systems are integrated to ensure optimal growth and immune responses?

2- What are the extracellular ROS sensors?

3- What are the molecular mechanisms of extracellular ROS perception?

We are taking a full advantage of the rapid developments in quantitative biochemistry, proteomics, systems and structural biology approaches to perform a large-scale receptor network and receptor-ligand pairing studies. This will be continued by in-depth mechanistic and physiological studies of key interactions/candidates.



PhD students

Sergio Martin Ramirez

Jente Stouthamer


Sjef Boeren


1. Kutschera A, Dawid C, Gisch N, Schmid Ch, Raasch L, Gerster T, Schäffer M, Smakowska-Luzan E, Belkhadir Y, Vlot AC, Chandler CE, Schellenberger R, Schwudke D, Ernst RK, Dorey S, Hückelhoven R, Hofmann T, Ranf S (2019). Bacterial medium chain 3-hydroxy fatty acid metabolites trigger immunity in Arabidopsis plants. Science, 364, 6436, pp. 178-181, DOI: 10.1126/science.aau1279

2. Mott GA*, Smakowska-Luzan E*, Pasha A, Parys K, Howton TC, Neuhold J, Lehner A, Grunwald K, Stolt-Bergner P, Provart NJ, Mukhtar MS, Desveaux D, Guttman DS, Belkhadir Y (2019). Map of physical interactions between extracellular domains of Arabidopsis leucine-rich repeat receptor kinases. Scientific Data, volume 6, article number: 190025 (2019) DOI: 10.1038/sdata.2019.25

* These authors contributed equally to this work

3. Smakowska-Luzan E, Mott GA, Parys K, Stegmann M, Howton TC, Layeghifard M, Neuhold J, Lehner A, Kong J, Grünwald K, Weinberger N, Satbhai SB, Mayer D, Busch W, Madalinski M, Stolt-Bergner P, Provart NJ, Mukhtar MS, Zipfel C, Desveaux D, Guttman DS, Belkhadir Y. (2018) An extracellular network of Arabidopsis leucine-rich repeat receptor kinases. Nature. 2018 Jan 18;553(7688):342-346. DOI: 10.1038/nature25184

4. Doblas V, Smakowska-Luzan E, Fujita S, Alassimone J, Barberon M, Madalinski M, Belkhadir Y* and Geldner N* (2017) Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor. Science. Jan 20;355(6322):280-284. DOI: 10.1126/science. aaj1562

5. Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A, Holton N, Belkhadir Y, Zipfel Y. (2017) The malectin-like receptor kinase FER is a RALF-regulated scaffold controlling plant immune signalling. Science. Jan 20;355(6322):287-289. DOI: C.1126/science. aal2541

6. Mott GA, Thakur S, Smakowska E, Wang PW, Belkhadir Y, Desveaux D, Guttman DS. (2016) Genomic screens identify a new phytobacterial microbe-associated molecular pattern and the cognate Arabidopsis receptor-like kinase that mediates its immune elicitation. Genome Biol. May 9;17(1):98. DOI: 10.1186/s13059-016-0955-7;

7. Saur IM, Kadota Y, Sklenar J, Holton NJ, Smakowska E, Belkhadir Y, Zipfel C, Rathjen JP. (2016) NbCSPR underlies age-dependent immune responses to bacterial cold shock protein in Nicotiana benthamiana. PNAS. Mar 22;113(12):3389-94. DOI: 10.1073/pnas.1511847113;

8. Smakowska E, Kong J, Busch W, Belkhadir Y. (2016) Organ-specific regulation of growth-defense tradeoffs by plants. Curr Opin Plant Biol. Feb; 29:129-37 DOI: 10.1016/j.pbi.2015.12.005;

9. Smakowska E, Skibior-Blaszczyk R, Czarna M, Kolodziejczak M, Kwasniak-Owczarek M, Parys K, Funk Ch, Janska H. (2016) Lack of FTSH4 protease affects protein carbonylation, mitochondrial morphology and phospholipid content in mitochondria of Arabidopsis: new insights into a complex interplay. Plant Physiol. Aug;171(4):2516-35. DOI: 10.1104/pp.16.00370;

10. Smakowska E, Czarna M, Janska H (2014) Mitochondrial ATP-dependent proteases in protection against accumulation of carbonylated proteins. Mitochondrion Mar 21. DOI: 10.1016/j.mito.2014.03.005;