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

Abstract

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.

Network Analysis Reveals a Common Host–Pathogen Interaction Pattern in Arabidopsis Immune Responses

“…In wrky72 mutant and recognition of peronospora parasitica 4 (rpp4) mutant, more susceptible phenotypes are conferred in response to Hpa infection (Bhattarai et al, 2010; Wang W. et al, 2011). In contrast, microtubule-associated protein 65-3 (map65-3) and phytosulfokin receptor 1 (pskr1) mutants show enhanced disease tolerance to Hpa (Quentin et al, 2016; Rodiuc et al, 2016). …”

A Plant Phytosulfokine Peptide Initiates Auxin-Dependent Immunity through Cytosolic Ca2+ Signaling in Tomato

“…The data presented here demonstrated the absence of significant changes in SA or JA levels or in the transcript accumulation of marker genes related to the signaling pathways of these phytohormones following PSK application ( Figures 3A and 3B). A previous transcriptome study using Arabidopsis gain-of-function overexpressing lines and loss-offunction mutants also report that signaling through PSKR1 does not significantly affect SA-or JA-related gene expression (Rodiuc et al, 2016). In addition, ET signaling is important in plant immunity against B. cinerea.…”

“…While auxin is a classical growth-regulating hormone in plants, it has been shown to positively modulate plant immunity in response to necrotrophic pathogens (Llorente et al, 2008;Kazan and Manners, 2009;Qi et al, 2012). SA has been suggested to be linked to PSK signaling, attenuating responses to the hemibiotrophic P. syringae and pathogen-associated molecular patterns (Igarashi et al, 2012;Mosher et al, 2013;Rodiuc et al, 2016). However, few studies have investigated PSK-induced phytohormone modulation in plant-necrotrophic pathogen interactions.…”

“…Considerable crosstalk between PSK signaling pathways and hormone pathways has been suggested to occur in the regulation of plant growth and stress responses (Eun et al, 2003;Mosher et al, 2013;Wu et al, 2015;Rodiuc et al, 2016). Therefore, we analyzed the relative levels of pathogen defense-related hormones (Glazebrook, 2005;Kazan and Manners, 2009) under mock-and B. cinereainoculated conditions.…”

“…PSK signaling pathways frequently act together with phytohormones to fine-tune plant responses to external and metabolic stimuli via interactions that can be either synergistic or antagonistic (Mosher et al, 2013;Rodiuc et al, 2016). For example, PSKR1 decreases the resistance of Arabidopsis plants to the hemibiotrophic bacterial pathogen Pseudomonas syringae but enhances defenses against the necrotrophic fungal pathogen Alternaria brassicicola.…”