Natural genetic resources of Arabidopsis thaliana reveal a high prevalence and unexpected phenotypic plasticity of RPW8‐mediated powdery mildew resistance

Abstract

Summary• Here, an approach based on natural genetic variation was adopted to analyse powdery mildew resistance in Arabidopsis thaliana.• Accessions resistant to multiple powdery mildew species were crossed with the susceptible Col-0 ecotype and inheritance of resistance was analysed. Histochemical staining was used to visualize archetypal plant defence responses such as callose deposition, hydrogen peroxide accumulation and host cell death in a subset of these ecotypes.• In six accessions, resistance was likely of polygenic origin while 10 accessions exhibited evidence for a single recessively or semi-dominantly inherited resistance locus. Resistance in the latter accessions was mainly manifested at the terminal stage of the fungal life cycle by a failure of abundant conidiophore production. The resistance locus of several of these ecotypes was mapped to a genomic region containing the previously analysed atypical RPW8 powdery mildew resistance genes. Gene silencing revealed that members of the RPW8 locus were responsible for resistance to Golovinomyces orontii in seven accessions.• These results suggest that broad-spectrum powdery mildew resistance in A. thaliana is predominantly of polygenic origin or based on RPW8 function. The findings shed new light on the natural variation of inheritance, phenotypic expression and pathogen range of RPW8-conditioned powdery mildew resistance.

The Powdery Mildew Disease of Arabidopsis: A Paradigm for the Interaction between Plants and Biotrophic Fungi

“…Efforts in dissecting resistance to powdery mildews in Arabidopsis have exploited the natural variation in resistance phenotypes among several hundred accessions collected worldwide (Adam and Somerville, 1996;Adam et al, 1999;Göllner et al, 2008). In most accessions analyzed to date resistance is either polygenic, based on the atypical resistance (R) gene RESISTANCE TO POWDERY MILDEW 8 (RPW8), or on combinations thereof, with RPW8 representing the major Quantitative Trait Locus (Adam and Somerville, 1996;Xiao et al, 1997;Adam et al, 1999;Wilson et al, 2001;Orgil et al, 2007;Göllner et al, 2008; Figure 1A-C, Figure 7).…”

“…Erysiphe) orontii are powdery mildews of cucurbits and crucifers that are able to infect Arabidopsis (Table 1). In addition, the less-extensively characterized tomato powdery mildew pathogen Oidium neolycopersici can successfully reproduce on Arabidopsis Ellis and Turner, 2001;Jones et al, 2001;Göllner et al, 2008;Whipps et al, 1998;Xiao et al, 2001; Table 1). Although all aforementioned species can colonize Arabidopsis under controlled laboratory conditions, the fungal species range, frequency and intensity of infections in natural Arabidopsis habitats has, to our knowledge, not been studied.…”

“…In most accessions analyzed to date resistance is either polygenic, based on the atypical resistance (R) gene RESISTANCE TO POWDERY MILDEW 8 (RPW8), or on combinations thereof, with RPW8 representing the major Quantitative Trait Locus (Adam and Somerville, 1996;Xiao et al, 1997;Adam et al, 1999;Wilson et al, 2001;Orgil et al, 2007;Göllner et al, 2008; Figure 1A-C, Figure 7). In general, more accessions are resistant to E. cruciferarum (76%) than to G. cichoracearum (63%) (Adam et al, 1999), while out of 64 accessions tested in an independent study, only 26% were resistant to G. orontii (Göllner et al, 2008). These numbers may reflect the degree of adaptation that each of these powdery mildew species possesses to cope with the variations of the antifungal defense repertoire that is common in natural Arabidopsis populations.…”

“…Note the difference in appearance of infected leaves of resistant accessions Do-0 and Sorbo. Resistance in both accessions is assumed to be governed by RPW8 (Göllner et al, 2008). species, attacked cells react to penetration attempts through the formation of CWAs (Figure 6), which -despite sparse experimental evidence supporting this view -are commonly thought to provide both physical cell wall reinforcements as well as a chemical anti-microbial blockade against the invading pathogen (reviewed in Hardham et al, 2007 andHückelhoven, 2007). Papillae are formed within a few hours after fungal penetration attempts in response to adapted and non-adapted pathogens.…”

Genetics and molecular mechanisms of resistance to powdery mildews in tomato (Solanum lycopersicum) and its wild relatives

“…The RPW8-mediated resistance present in several other Arabidopsis accessions seems to be non-functional against O. neolycopersici. Instead, at least two other major loci in the accession Bay-0 appear to mediate such a resistance (Göllner et al 2008), demonstrating that genetic factors in Arabidopsis for resistance to O. neolycopersici are different from those to Golovinomyces spp. Very likely, O. neolycopersici delivers effector(s) that is/are different from the ones delivered by Golovinomyces spp.…”