Gene-for-Gene Tolerance to Bacterial Wilt in Arabidopsis

Abstract

Bacterial wilt caused by Ralstonia solanacearum is a disease of widespread economic importance that affects numerous plant species, including Arabidopsis thaliana. We describe a pathosystem between A. thaliana and biovar 3 phylotype I strain BCCF402 of R. solanacearum isolated from Eucalyptus trees. A. thaliana accession Be-0 was susceptible and accession Kil-0 was tolerant. Kil-0 exhibited no wilting symptoms and no significant reduction in fitness (biomass, seed yield, and germination efficiency) after inoculation with R. solanacearum BCCF402, despite high bacterial numbers in planta. This was in contrast to the well-characterized resistance response in the accession Nd-1, which limits bacterial multiplication at early stages of infection and does not wilt. R. solanacearum BCCF402 was highly virulent because the susceptible accession Be-0 was completely wilted after inoculation. Genetic analyses, allelism studies with Nd-1, and RRS1 cleaved amplified polymorphic sequence marker analysis showed that the tolerance phenotype in Kil-0 was dependent upon the resistance gene RRS1. Knockout and complementation studies of the R. solanacearum BCCF402 effector PopP2 confirmed that the tolerance response in Kil-0 was dependent upon the RRS1-PopP2 interaction. Our data indicate that the gene-for-gene interaction between RRS1 and PopP2 can contribute to tolerance, as well as resistance, which makes it a useful model system for evolutionary studies of the arms race between plants and bacterial pathogens. In addition, the results alert biotechnologists to the risk that deployment of RRS1 in transgenic crops may result in persistence of the pathogen in the field.

The Coevolutionary Implications of Host Tolerance

“…One study found evidence of a GFG like interaction for tolerance to bacterial wilt in Arabidopsis conferred by a single R‐gene (Van der Linden et al. ), but such specificities might also be effectively modeled by a tolerance range function. Overall, however, our results have emphasized that whatever the model structure, the coevolutionary interaction of hosts and parasites is not in itself enough to generate diversity in host tolerance.…”

Ralstonia solanacearum, a widespread bacterial plant pathogen in the post‐genomic era

“…In A. thaliana, the study of the interaction between two ecotypes, Nd-1 and Kil-0, and two strains of R. solanacearum, GMI1000 and BCCF402 (both phylotype I strains), respectively, revealed the involvement of RRS1-R. RRS1-R, a Toll/interleukin-1 receptor-nucleotide-binding siteleucine-rich repeat (TIR-NBS-LRR) gene with a WRKY C-terminal domain, has been described as a single recessive resistance gene against strain GMI1000, through the direct recognition of the PopP2 effector (Deslandes et al, 1998(Deslandes et al, , 2003. Interestingly, it has been demonstrated recently that the gene-for-gene interaction RRS1-R-PopP2 is also involved in Kil-0 tolerance ( Van der Linden et al, 2013). Indeed, Kil-0 does not exhibit wilting symptoms after its inoculation with strain BCCF402 of R. solanacearum, despite a high bacterial multiplication in planta.…”

Mapping QTL conferring resistance in maize to gray leaf spot disease caused by Cercospora zeina

“…However, since the molecular basis of resistance to GLS has not been characterized yet, it still remains possible that quantitative resistance could be effected by so-called weak resistance (R) genes that recognize pathogen effectors in a gene-for-gene manner [18]. A mechanism for this could be tolerance mediated through an R gene, as was recently shown in Arabidopsis pathosystems [19,20]. …”