Priming of plant defence against pathogens and herbivores by DNA damage signalling

Principal Investigator: Dr. Lennart Wirthmüller

Plants evolved a versatile immune system that mediates defence against a plethora of pathogens with different infection strategies. The molecular signalling cascades that relay pathogen perception from the plasma membrane to transcriptional upregulation of defence genes in the nucleus are well characterised. In contrast it remains poorly understood how plants store information on previous infections and how this allows them to respond faster or with greater amplitude to re-occurring attack. Recent findings demonstrate that accumulation of DNA double strand (ds) breaks and activation of the molecular DNA damage response (DDR) in host plants are common events associated with infection by both (hemi-)biotrophic and necrotrophic pathogens. Genetically, priming of salicylic acid (SA)-dependent immunity requires several DDR components, substantiating the link between the two signalling pathways.

The objective of this project is to test the hypothesis that pathogen-induced DNA damage and activation of DDR signalling in infected cells contribute to short-term memory of infection and mediate priming of plant defence genes. In support of this hypothesis we have demonstrated that pre-treatment of Arabidopsis thaliana with the DNA ds break-inducing glycopeptide bleomycin primes the expression of SA-responsive defence genes over several days. We will perform transcriptome profiling to determine which defence genes are primed by sensing DNA damage and correlate ‘primability’ of these genes with levels of histone H3 tri-methylation on Lys4 (H3K4me3), which has been associated with transcriptional memory of biotic and abiotic stress. Furthermore we will test if accumulation of SA is required for priming of selected defence genes. We will screen a set of combinatorial DDR mutants impaired in distinct ‘layers’ of DNA repair for priming and resistance against a bacterial pathogen and determine which DDR repair pathways are essential for bleomycin-mediated defence gene priming.

To address if DDR signalling also plays a role in priming anti-herbivore defences we will extend our studies to oviposition-mediated priming of resistance against larval feeding on A. thaliana and elm (Ulmus minor). Recent studies in projects B4 (Arabidopsis) and B1 (elm) showed that oviposition on Arabidopsis and elm leaves induces a transcriptional response that shares significant overlap with transcriptome changes induced by hemi-biotrophic pathogens. We will test if DNA ds breaks and DDR signalling are induced by oviposition. Furthermore we will test Arabidopsis combinatorial DDR mutants for altered oviposition-mediated priming of resistance against larval feeding.

Overall this project will address the role of attacker-elicited DDR signalling in priming of plant defences against biotic stressors.

References

Asai, S., Rallapalli, G., Piquerez, S. J. , Caillaud, M. C., Furzer, O. J., Ishaque, N., Wirthmueller, L.,Fabro, G., Shirasu, K., Jones J. D. 2014. Expression profiling during Arabidopsis/downy mildew interaction reveals a highly-expressed effector that attenuates responses to salicylic acid. PLoS Pathog. 10:e1004443.

Caillaud, M.C.*, Wirthmueller, L.*, Sklenar, J., Findlay, K., Piquerez, S.J., Jones, A. M., Robatzek, S., Jones, J. D., Faulkner, C. 2014. The plasmodesmal protein PDLP1 localises to haustoria-associated membranes during downy mildew infection and regulates callose deposition. PLoS Pathog. 10:e1004496.

Caillaud, M. C., Wirthmueller, L., Fabro, G., Piquerez, S. J., Asai, S., Ishaque, N., Jones, J. D. 2012. Mechanisms of nuclear suppression of host immunity by effectors from the Arabidopsis downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa). Cold Spring Harb. Symp. Quant. Biol. 77:285-293.

Genenncher B., Wirthmueller, L., Roth, C., Klenke, M., Ma, L., Sharon, A., Wiemer, M. 2016. Nucleoporin-regulated MAP kinase signaling in immunity to a necrotrophic fungal pathogen. Plant Physiol. pii:pp.00832.2016. [Epub ahead of print]

Heidrich, K., Wirthmueller, L., Tasset, C., Pouzet, C., Deslandes, L., Parker J.E. 2011. Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science334:1401-1404.

Heidrich, K., Tsuda, K., Blanvillain-Baufumé, S., Wirthmueller, L., Bautor, J., Parker, J. E. 2013. Arabidopsis TNL-WRKY domain receptor RRS1 contributes to temperature-conditioned RPS4 auto-immunity. Front. Plant Sci. 4:403.

Sarris, P.F., Duxbury, Z., Huh, S. U., Ma, Y., Segonzac, C., Sklenar, J., Derbyshire, P., Cevik, V., Rallapalli, G., Saucet, S. B., Wirthmueller, L., Menke, F. L., Sohn, K. H., Jones, J. D. 2015. Immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161:1089-1100.

Wirthmueller, L., Roth, C., Fabro, G., Caillaud, M. C., Rallapalli, G., Asai, S., Sklenar, J., Jones, A. M., Wiermer, M., Jones, J. D., Banfield M. J. 2015. Probing formation of cargo/importin-α transport complexes in plant cells using a pathogen effector. Plant J. 81:40-52.

Wirthmueller, L.*, Maqbool, A.*, Banfield, M. J. 2013. On the front line: structural insights into plant-pathogen interactions. Nat. Rev. Microbiol. 11:761-776.

Wirthmueller, L., Zhang, Y., Jones, J. D., Parker, J. E. 2007. Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Curr. Biol. 17:2023-2029.