Modulation ofACD6dependent hyperimmunity by natural alleles of anArabidopsis thalianaNLR resistance gene

Abstract

Plants defend themselves against pathogens by activating an array of immune responses.Unfortunately, immunity programs may also cause unintended collateral damage to the plant itself.The quantitative disease resistance gene ACCELERATED CELL DEATH 6 (ACD6) serves as a nexus for the trade-off between growth and pathogen resistance in wild populations of Arabidopsis thaliana. An autoimmune allele, ACD6-Est, first identified in the natural accession Est-1, is found in over 10% of wild strains, even though it causes a clear fitness penalty under optimal growth conditions. There is, however, extensive variation in the strength of the autoimmune phenotype expressed by strains with an ACD6-Est allele, indicative of genetic modifiers. Quantitative genetic analysis suggests that the population genetic basis of ACD6 modulation is complex, with different strains often carrying different large-effect modifiers. One modifier is SUPPRESSOR OF NPR1-1, CONSTITUTIVE 1 (SNC1), located in a highly polymorphic cluster of nucleotide-binding domain and leucine-rich repeat (NLR) immune receptor genes, which are prototypes for qualitative disease resistance genes. Allelic variation at SNC1 correlates with ACD6-Est activity in multiple accessions, and a common structural variant affecting the NL linker sequence can explain differences in SNC1 activity. Taken together, we find that an NLR gene can mask the activity of an ACD6 autoimmune allele in natural A. thaliana populations, thereby linking different arms of the plant immune system. Author summaryPlants defend themselves against pathogens by activating immune responses. Unfortunately, these can cause unintended collateral damage to the plant itself. Nevertheless, some wild plants have genetic variants that confer a low threshold for the activation of immunity. While these enable a plant to respond particularly quickly to pathogen attack, such variants might be potentially dangerous. We are investigating one such variant of the immune gene ACCELERATED CELL DEATH 6 (ACD6) in the plant Arabidopsis thaliana. We discovered that there are variants at other genetic loci that can mask the effects of an overly active ACD6 gene. One of these genes, SUPPRESSOR OF NPR1-1, CONSTITUTIVE 1 (SNC1), codes for a known immune receptor. The SNC1 variant that attenuates ACD6 activity is rather common in A. thaliana populations, suggesting that new combinations of the hyperactive ACD6 variant and this antagonistic SNC1 variant will often arise by natural crosses. Similarly, because the two genes are unlinked, outcrossing will often lead to the hyperactive ACD6 variants being unmasked again. We propose that allelic diversity at SNC1 contributes to the maintenance of the hyperactive ACD6 variant in natural A. thaliana populations.Zhu, Zaidem et al.:Natural ACD6 modulator

Plant immunity in signal integration between biotic and abiotic stress responses

“…It is of interest to determine whether this CAMTA function is distinct from the transcriptional regulation mentioned earlier, and, if so, how it is mechanistically achieved. Genetic modifiers underlie the species-wide spread of autoimmune hyperactive alleles of the ER and plasma membrane-resident SA regulator ACD6 in A. thaliana, despite marked MPK3/MPK6 activation and growth retardation (Todesco et al, 2010;Tateda et al, 2014;Zhu et al, 2018). Allelic diversity of SNC1 provides a basis to restrict ACD6 activity and cell death.…”

ARADEEPOPSIS, an Automated Workflow for Top-View Plant Phenomics using Semantic Segmentation of Leaf States

“…The highest-ranking SNP in this region was located within the coding region of ACCELERATED CELL DEATH 6 (ACD6; At4g14400) ( Figure 6C). ACD6 has been extensively studied in Arabidopsis and was identified as being associated with vegetative growth, microbial resistance, and necrosis (Atwell et al, 2010;Todesco et al, 2010;Zhu et al, 2018). Our plants were grown on natural, non-sterilized soil from a field site near Zurich, Switzerland (Hu et al, 2018); it is therefore fair to assume that the microbial load and potential biotic stress levels were higher than in standard potting soil.…”

Arabidopsis thaliana natural variation in temperature-modulated immunity uncovers transcription factor UNE12 as a thermoresponsive regulator

“…3a-b), points to genotypic variation in the threshold at which SA leads to autoimmunity 23 . Presence of genetic modifiers of SA-related autoimmunity and stress sensitivity are evident from studies of different A. thaliana accessions 35, 59 . Alterations in the hormone network controlling SA crosstalk with growth-promoting pathways might buffer against SA negative effects in some genotypes 60 .…”