Invasion of the stigma by oomycete pathogenic hyphae or pollen tubes : striking similarities and differences.

Both filamentous pathogens' hyphae and pollen tube penetrate the host's outer layer and involve growth within the host tissues. Early epidermal responses are decisive for the outcome of these two-cell interaction processes. We identified a single cell type, the papilla of Arabidospis thaliana's stigma, as a tool to conduct a comprehensive comparative analysis on how an epidermal cell responds to the invasion of an unwanted pathogen or a welcomed pollen tube. We showed that Phytophtora parasitica, a root oomycete, effectively breaches the stigmatic cell wall and develops as a biotroph within the papilla cytoplasm. These invasive features resemble the behaviour exhibited by the pathogen within its natural host cells, but diverge from the manner in which the pollen tube progresses, being engulfed within the papilla cell wall. Quantitative analysis revealed that both invaders trigger reorganisation of the stigmatic endomembrane system and the actin cytoskeleton. While some remodelling processes are shared between the two interactions, others appear more specific towards the respective invader. These findings underscore the remarkable ability of an epidermal cell to differentiate between two types of invaders, thereby enabling it to trigger the most suitable response during the onset of invasion.

A plant receptor domain with functional analogies to animal malectin disables ER stress responses upon infection.

Malectins from the oligosaccharyltransferase (OST) complex in the endoplasmic reticulum (ER) of animal cells are involved in ER quality control and contribute to the Unfolded Protein Response (UPR). Malectins are not found in plant cells, but malectin-like domains (MLDs) are constituents of many membrane-bound receptors. In Arabidopsis thaliana, the MLD-containing receptor IOS1 promotes successful infection by filamentous plant pathogens. We show that the MLD of its exodomain retains IOS1 in the ER of plant cells and attenuates the infection-induced UPR. Expression of the MLD in the ios1-1 knockout background is sufficient to complement infection-related phenotypes of the mutant, such as increased UPR and reduced disease susceptibility. IOS1 interacts with the ER membrane-associated ribophorin HAP6 from the OST complex, and hap6 mutants show decreased pathogen-responsive UPR and increased disease susceptibility. Altogether, this study revealed a previously uncharacterized role of a plant receptor domain in the regulation of ER stress during infection.

Evolutionarily distant pathogens require the Arabidopsis phytosulfokine signalling pathway to establish disease.

Secreted peptides and their specific receptors frequently orchestrate cell-to-cell communication in plants. Phytosulfokines (PSKs) are secreted tyrosine-sulphated peptide hormones, which trigger cellular dedifferentiation and redifferentiation upon binding to their membrane receptor. Biotrophic plant pathogens frequently trigger the differentiation of host cells into specialized feeding structures, which are essential for successful infection. We found that oomycete and nematode infections were characterized by the tissue-specific transcriptional regulation of genes encoding Arabidopsis PSKs and the PSK receptor 1 (PSKR1). Subcellular analysis of PSKR1 distribution showed that the plasma membrane-bound receptor internalizes after binding of PSK-α. Arabidopsis pskr1 knockout mutants were impaired in their susceptibility to downy mildew infection. Impaired disease susceptibility depends on functional salicylic acid (SA) signalling, but not on the massive up-regulation of SA-associated defence-related genes. Knockout pskr1 mutants also displayed a major impairment of root-knot nematode reproduction. In the absence of functional PSKR1, giant cells arrested their development and failed to fully differentiate. Our findings indicate that the observed restriction of PSK signalling to cells surrounding giant cells contributes to the isotropic growth and maturation of nematode feeding sites. Taken together, our data suggest that PSK signalling in Arabidopsis promotes the differentiation of host cells into specialized feeding cells.

The receptor kinase IMPAIRED OOMYCETE SUSCEPTIBILITY1 attenuates abscisic acid responses in Arabidopsis.

In plants, membrane-bound receptor kinases are essential for developmental processes, immune responses to pathogens and the establishment of symbiosis. We previously identified the Arabidopsis (Arabidopsis thaliana) receptor kinase IMPAIRED OOMYCETE SUSCEPTIBILITY1 (IOS1) as required for successful infection with the downy mildew pathogen Hyaloperonospora arabidopsidis. We report here that IOS1 is also required for full susceptibility of Arabidopsis to unrelated (hemi)biotrophic filamentous oomycete and fungal pathogens. Impaired susceptibility in the absence of IOS1 appeared to be independent of plant defense mechanism. Instead, we found that ios1-1 plants were hypersensitive to the plant hormone abscisic acid (ABA), displaying enhanced ABA-mediated inhibition of seed germination, root elongation, and stomatal opening. These findings suggest that IOS1 negatively regulates ABA signaling in Arabidopsis. The expression of ABA-sensitive COLD REGULATED and RESISTANCE TO DESICCATION genes was diminished in Arabidopsis during infection. This effect on ABA signaling was alleviated in the ios1-1 mutant background. Accordingly, ABA-insensitive and ABA-hypersensitive mutants were more susceptible and resistant to oomycete infection, respectively, showing that the intensity of ABA signaling affects the outcome of downy mildew disease. Taken together, our findings suggest that filamentous (hemi)biotrophs attenuate ABA signaling in Arabidopsis during the infection process and that IOS1 participates in this pathogen-mediated reprogramming of the host.

An Arabidopsis (malectin-like) leucine-rich repeat receptor-like kinase contributes to downy mildew disease.

Biotrophic filamentous plant pathogens frequently establish intimate contact with host cells through intracellular feeding structures called haustoria. To form and maintain these structures, pathogens must avoid or suppress defence responses and reprogramme the host cell. We used Arabidopsis whole-genome microarrays to characterize genetic programmes that are deregulated during infection by the biotrophic' oomycete downy mildew pathogen, Hyaloperonospora arabidopsidis. Marked differences were observed between early and late stages of infection, but a gene encoding a putative leucine-rich repeat receptor-like kinase (LRR-RLK) was constantly up-regulated. We investigated the evolutionary history of this gene and noticed it being one of the first to have emerged from a common ancestral gene that gave rise to a cluster of 11 genes through duplications. The encoded LRR-RLKs harbour an extracellular malectin-like (ML) domain in addition to a short stretch of leucine-rich repeats, and are thus similar to proteins from the symbiosis receptor-like kinase family. Detailed expression analysis showed that the pathogen-responsive gene was locally expressed in cells surrounding the oomycete. A knockout mutant showed reduced downy mildew infection, but susceptibility was fully restored through complementation of the mutation, suggesting that the (ML-)LRR-RLK contributes to disease. According to the mutant phenotype, we denominated it Impaired Oomycete Susceptibility 1 (IOS1).

Getting the most from the host: how pathogens force plants to cooperate in disease.

Plant diseases caused by pathogenic microorganisms remain a major limitation in many crop production systems. Nonetheless, constitutive and inducible defense mechanisms render most plants inaccessible to pathogens, making disease an exception rather than a common outcome of plant-microbe interactions. Defense mechanisms and associated pathogen resistance were thus of key interest to many plant pathologists, and many of the molecular mechanisms underlying resistance have been elucidated over the last few decades. In recent years, the analysis of physiological and molecular determinants accounting for successful infection and eventual disease has become a topic of prime scientific interest. The hunt is now on for pathogen effectors subverting the host cell and for the plant compatibility functions manipulated by these effectors. An understanding of the molecular mechanisms underlying successful infection should make it possible to develop new crop protection strategies based on interference with compatibility to prevent disease. This review is addressing plant susceptibility and highlights a number of host processes that have been shown to be induced or subverted to facilitate infection. In particular, we focus on those processes that appear to be manipulated by filamentous fungal and oomycete pathogens.