Abstract
Interactions between Arabidopsis thaliana and its native obligate oomycete pathogen Hyaloperonospora arabidopsidis (Hpa) represent a model system to study evolution of natural variation in a host/pathogen interaction. Both Arabidopsis and Hpa genomes are sequenced and collections of different sub-species are available. We analyzed ∼400 interactions between different Arabidopsis accessions and five strains of Hpa. We examined the pathogen's overall ability to reproduce on a given host, and performed detailed cytological staining to assay for pathogen growth and hypersensitive cell death response in the host. We demonstrate that intermediate levels of resistance are prevalent among Arabidopsis populations and correlate strongly with host developmental stage. In addition to looking at plant responses to challenge by whole pathogen inoculations, we investigated the Arabidopsis resistance attributed to recognition of the individual Hpa effectors, ATR1 and ATR13. Our results suggest that recognition of these effectors is evolutionarily dynamic and does not form a single clade in overall Arabidopsis phylogeny for either effector. Furthermore, we show that the ultimate outcome of the interactions can be modified by the pathogen, despite a defined gene-for-gene resistance in the host. These data indicate that the outcome of disease and disease resistance depends on genome-for-genome interactions between the host and its pathogen, rather than single gene pairs as thought previously.
Highlights
Hyaloperonospora arabidopsidis (Hpa, formerly known as Peronospora parasitica) is a native downy mildew pathogen of the plant model organism Arabidopsis thaliana [1,2]
We examined interactions between 83 accessions of Arabidopsis thaliana, collected from diverse locations around the world [15], and five strains of Hyaloperonospora arabidopsidis (Hpa) originally isolated in the United Kingdom [3]
Our analysis indicates that Hpa Emco5 successfully colonized 42% of Arabidopsis cotyledons, comparable to other strains used in this study (Table 1)
Summary
Hyaloperonospora arabidopsidis (Hpa, formerly known as Peronospora parasitica) is a native downy mildew pathogen of the plant model organism Arabidopsis thaliana [1,2]. Hpa is an obligate biotrophic pathogen, propagating to a new host by means of small asexual conidiospores that form on sporangiophores emerging from the plant leaf surface after successful colonization of plant leaf tissues. Sexual oospores form inside the plant, generating genetic diversity for the pathogen [1]. Host plant defense responses are induced shortly after the pathogen starts to grow. A visible hallmark of plant defense is the induction of the hypersensitive cell-death response [1]. The obligate nature of the interactions between Hpa and Arabidopsis has brought evolutionary pressure on both the pathogen and the host. Similar evolutionary patterns have been observed for many Arabidopsis disease resistance genes, which occur in multiple copies at complex genetic loci [4,8]. Understanding the genetic and phenotypic diversity of Arabidopsis/
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