Expression polymorphism at the ARPC4 locus links the actin cytoskeleton with quantitative disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana

Abstract

Quantitative disease resistance (QDR) is a form of plant immunity widespread in nature, and the only one active against broad host range fungal pathogens. The genetic determinants of QDR are complex and largely unknown, and are thought to rely partly on genes controlling plant morphology and development.We used genome-wide association mapping in Arabidopsis thaliana to identify ARPC4 as associated with QDR against the necrotrophic fungal pathogen Sclerotinia sclerotiorum. Mutants impaired in ARPC4 showed enhanced susceptibility to S. sclerotiorum, defects in the structure of the actin filaments and in their responsiveness to S. sclerotiorum. Disruption of ARPC4 also alters callose deposition and the expression of defense-related genes upon S. sclerotiorum infection.Analysis of ARPC4 diversity in A. thaliana identified one haplotype (ARPC4 R ) showing a c. 1 kbp insertion in ARPC4 regulatory region and associated with higher level of QDR. Accessions from the ARPC4 R haplotype showed enhanced ARPC4 expression upon S. sclerotiorum challenge, indicating that polymorphisms in ARPC4 regulatory region are associated with enhanced QDR.This work identifies a novel actor of plant QDR against a fungal pathogen and provides a prime example of genetic mechanisms leading to the recruitment of cell morphology processes in plant immunity.480 New Phytologist (2019) 222: 480-496

Phylotranscriptomics of the Pentapetalae Reveals Frequent Regulatory Variation in Plant Local Responses to the Fungal Pathogen Sclerotinia sclerotiorum

“…Although 47% of DEGs belonged to core orthogroups conserved in six plant species, only 2.01% of core orthogroups contained genes upregulated in six species (and 3.56% genes down-regulated in six species), highlighting frequent regulatory variation within orthogroups. In our previous work, we identified allelic variants of the ARPC4 gene differing in their promoter region, induction upon pathogen challenge, and associated with resistance to S. sclerotiorum (Badet et al, 2019). These findings are in line with a prominent role of regulatory variation in the evolution of QDR.…”

“…In some A. thaliana accessions, insertion of a TE-derived enhancer mediated WRKY33 binding to the promoter of the CYP82C2 gene, making it inducible upon bacterial pathogen inoculation, activating biosynthesis of the antimicrobial 4-hydroxyindole-3-carbonylnitrile metabolite (Barco et al, 2019). A similar mechanism could have driven the emergence of a S. sclerotiorum-inducible allele of ARPC4 associated with enhanced QDR in A. thaliana (Badet et al, 2019). The pangenomic repertoire of QDR transcripts conserved across species but differentially regulated upon S. sclerotiorum inoculation provide an original resource for the identification of new transcription enhancer motifs.…”

“…sclerotiorum (Badet et al, 2017(Badet et al, , 2019Barbacci et al, 2018;Derbyshire et al, 2019). The inactivation of these genes caused 16 to 36% variation in the QDR phenotype each, in line with previous quantitative trait loci analyses for QDR in crops (Micic et al, 2004;Poland et al, 2011;Bonhomme et al, 2014).…”

“…In the harlequin ladybird beetle (Harmonia axyridis), allelic variation in the cis-regulatory region of the transcription factor gene pannier is responsible for over 200 distinct patterns of red and black on the elytra (the hardened forewing), providing a striking example of phenotypic variation caused by cis-regulatory variants at the intraspecific level (Ando et al, 2018;Gautier et al, 2018). In our previous work, we showed that the ARPC4 gene encoding an actin-related protein complex member controls the dynamics of the actin filament network with an impact on QDR against S. sclerotiorum (Badet et al, 2019). Two major alleles of ARPC4 were detected in A. thaliana populations, associated with contrasted levels of QDR.…”

Disrupted actin: a novel player in pathogen attack sensing?

“…We believe that future research can benefit hugely from natural variation studies. Indeed, a genome‐wide associated study (GWAS) based on the screening of susceptibility to Sclerotinia sclerotiorum has already highlighted ARPC4, a new player involved in quantitative disease resistance and an actin organization regulator, both in the resting state and in response to infection (Badet et al , 2019). Forward genetics can also be fruitful.…”