Nuclear Activities of DNA-Associated Immune Receptors

• Applicants: Professor Dr. Karsten Niefind; Professorin Dr. Jane E. Parker
• Subject Area: Organismic Interactions, Chemical Ecology and Microbiomes of Plant Systems ; Plant Biochemistry and Biophysics ; Plant Physiology ; Plant Cell and Developmental Biology
• Term: from 2015 to 2021
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 283906930

In innate immunity, pathogen interference is monitored inside cells by nucleotide-binding/leucine-rich-repeat receptors (NLRs). Plant NLRs recognize variable pathogen-derived effector proteins delivered into host cells. NLR receptors must be tightly controlled since misregulated NLRs can lead to autoimmunity. Although various NLR activation events are becoming more transparent, the mechanisms by which NLRs mobilize immunity pathways remain obscure. This proposal aims to elucidate receptor signaling dynamics at the chromatin during transcriptional reprogramming in effector-triggered immunity (ETI) controlled by a co-functioning Arabidopsis NLR pair, RRS1-R (RESISTANCE TO RALSTONIA SOLANACEARUM1) and RPS4 (RESISTANCE TO PSEUDOMONAS SYRINGAE4), that confers resistance among others to root-infecting Ralstonia solanacearum bacteria expressing a type-III secreted effector (T3SE), PopP2, and leaf-infecting Pseudomonas syringae bacteria secreting an unrelated T3SE, AvrRps4. Analyses of RRS1-R/RPS4 interactions suggest that a heterodimer represents a resting state which is activated by direct binding of PopP2 or AvrRps4 to RRS1-R. Recently, P1 (Deslandes) and P2 (Parker) elucidated the mechanism by which PopP2 triggers RRS1-R/RPS4 activation. PopP2 acetylation of a key lysine within the WRKY DNA-binding domain of RRS1-R disrupts RRS1-R DNA association and activates RPS4-dependent immunity. PopP2 employs this Lys acetylation strategy to target multiple defense-promoting WRKY transcription factors, causing loss of WRKY-DNA binding and transactivating functions needed for defense gene expression. Thus, RRS1-R represents a DNA-bound immune receptor with an integrated effector decoy, which directly converts an essential pathogen virulence activity into immunity (Cell, in press). RRS1-R/RPS4 immunity depends on ENHANCED DISEASE SENSITIVITY1 (EDS1), a basal immunity regulator interacting with PHYTOALEXIN DEFICIENT4 (PAD4) or SENESCENCE ASSOCIATED GENE1 (SAG101). By resolving the EDS1-SAG101 crystal structure, P2 and P3 (Niefind) recently explained the requirement of EDS1-PAD4 or EDS1-SAG101 complexes for Arabidopsis immunity. EDS1 that interacts with several NLRs is a candidate protein for transmission of signals from ETI immune complexes at the chromatin to the transcriptional reprogramming of cells. Presumably, RRS1-R anchors an RRS1-R/RPS4/EDS1 complex at specific chromatin sites and provides a chromatin context for transcriptional reprogramming. AvrRps4 and PopP2 activities might converge on a chromatin hub guarded by this immune receptor complex whose dislodging from DNA activates resistance pathways. Here, the P1, P2 and P3 partners bring together complementary expertise to pursue genetic, genomic and structural/biophysical approaches to unravel NLR dynamics at the DNA. This will uncover how the active state of NLRs connects to downstream signaling events and how these are integrated for host transcriptional defense responses.

• DFG Programme: Research Grants
• International Connection: France
• Partner Organisation: Agence Nationale de la Recherche / The French National Research Agency
• Cooperation Partner: Laurent Deslandes, Ph.D.