Much of what we’ve learned about plant innate immunity (- the nuts and bolts of the system) has come from characterizing induced responses to homogenous and often non-physiological levels of a particular microbial pathogen. It is unclear how relevant and penetrant these processes are in the field. Now that some of the key players in plant immunity and stress hormone signaling have been identified, we aim to get a fuller insight to how the plant manages its biotic stress network under more natural conditions in which maintaining a balance between effective disease resistance and metabolic homeostasis is crucial for survival and growth. In nature, the plant integrates numerous environmental cues such as temperature, light, drought, herbivory, competition from other plants. It also hosts structured communities of microorganisms in its leaves and roots which can be benign or even beneficial. How the plant is able to resist harmful fungi, bacteria or pests while maintaining potentially useful microbiota is not known. Our working hypothesis is that, in nature, the plant immune system shapes and is itself shaped by endophytic microbes and the methods and tools are now available to disentangle these interesting relationships.
We’re approaching this broader question in two studies. In the first, together with Eric Kemen (MPIPZ) and Rubén Alcázar (University of Barcelona), we’re characterizing natural Arabidopsis thaliana populations in and around the town of Gorzów-Wielkopolski in Poland. In some of these populations, an interesting complex locus of eight NLR (Dm2) genes has been maintained at moderate frequency in genetically different individuals. We have started to analyze the distribution of Dm2 and other NLR genes in the populations, and to isolate pathogens from the field. We have also begun sampling leaves of individual plants at the Gorzów sites for microbial epiphytes and endophytes on leaves over multiple years. Computational network analysis of leaf-associated microbiota combined with plant-microbe reconstitution assays in genetically defined Gw individuals under lab conditions will allow us to relate plant genotype with microbial community structure and ask whether NLR composition contributes to the structuring of microbial populations beyond determining local pathogen resistance.
In the second study, we’re examining the extent of natural variation in A. thaliana defence pathway homeostasis in response to two different ambient temperatures (20oC and 16oC) - essentially a genotype x environment (G x E) experiment within the normal range of this species. The analysis has uncovered extensive genetic variation in temperature-conditioned accumulation of the stress hormone SA, which correlates only poorly with plant growth. Our initial results suggest a large degree of genetic plasticity in the regulation of defence outputs and potential benefits of high SA levels in terms of increased pathogen resistance. We’re now using a combination of GWAS and QTL analysis to identify candidate genes underlying the SA x temp trait variation. We’re also investigating whether differences in SA pathway homeostasis can be explained at the level of molecular cross-talk within the plant stress hormone network. Finally, we will test how robust the differential G x E interactions are under field conditions.
Ariga H, Katori T, Tsuchimatsu T, Hirase T, Tajima Y, Parker JE, Alcázar R, Koornneef M, Hoekenga O, Lipka AE, Gore MA, Sakakibara H, Kojima M, Kobayashi Y, Iuchi S, Kobayashi M, Shinozaki K, Sakata Y, Hayashi T, Saijo Y and Taji T. 2017. NLR locus-mediated trade-off between abiotic and biotic stress adaptation in Arabidopsis. Nature Plants, in press.
Stuttmann J, Peine N, Garcia AV, Wagner C, Choudhury SR, Wang Y, James GV, Griebel T, Alcázar R, Tsuda K, Schneeberger K, Parker JE. 2016. Arabidopsis thaliana DM2h (R8) within the Landsberg RPP1-like Resistance locus underlies three different cases of EDS1-conditioned autoimmunity. PLoS Genet. 12: e1005990.
Alcazar R, von Reth M, Bautor J, Chae E, Weigel D, Koornneef M, Parker JE. 2014. Analysis of a plant complex resistance gene locus underlying immune-related hybrid incompatibility and its occurrence in nature. PloS Genet. 10, e1004848.
Gloggnitzer J, Akimcheva S, Srinivasan A, Kusenda B, Riehs N, Stampfl H, Bautor J, Dekrout B, Jonak C, Jiménez-Gómez J, Parker JE, Riha K. 2014. Nonsense-mediated mRNA decay modulates immune receptor levels to regulate plant antibacterial defense. Cell Host Microbe 16, 376-390.
Alcázar R and Parker JE. 2011. The impact of temperature on balancing immune responsiveness and growth in Arabidopsis. Trends Plant Sci. 16, 666-675.
Alcázar R, García AV, Kronholm I, de Meaux J, Koornneef M, Parker JE and Reymond M. 2010. Natural variation at Strubbelig Receptor Kinase 3 drives immune-triggered incompatibilities between A. thaliana accessions. Nature Genet. 42:1135-1139.
Alcázar R, Garcia AV, Parker JE and Reymond M. 2009. Incremental steps towards incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic pathway activation. Proc. Natl. Acad. Sci. USA 106: 334-339.