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.
INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Natalia
N
Rodiuc
Laboratoire des Interactions Plantes-Microorganismes, UMR CNRS 2594 - INRA 441, 31326, Castanet Tolosan, France.
Xavier
X
Barlet
INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Sophie
S
Hok
INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Laetitia
L
Perfus-Barbeoch
INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Valérie
V
Allasia
INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Gilbert
G
Engler
INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Aurélie
A
Séassau
INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Nathalie
N
Marteu
INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Janice
J
de Almeida-Engler
INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Franck
F
Panabières
INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Pierre
P
Abad
Department of Plant Biochemistry, Center for Plant Molecular Biology, University of Tübingen, 72076, Tübingen, Germany.
Birgit
B
Kemmerling
Laboratoire des Interactions Plantes-Microorganismes, UMR CNRS 2594 - INRA 441, 31326, Castanet Tolosan, France.
Yves
Y
Marco
INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Bruno
B
Favery
INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Harald
H
Keller
D000818:Animals; D017360:Arabidopsis / Q000378:metabolism / Q000382:microbiology*; D029681:Arabidopsis Proteins / Q000378:metabolism*; D004705:Endocytosis; D054884:Host-Pathogen Interactions; D009868:Oomycetes / Q000502:physiology*; D036361:Peptide Hormones / Q000378:metabolism; D010935:Plant Diseases; D010940:Plant Proteins / Q000378:metabolism; D018517:Plant Roots / Q000502:physiology; D043368:Ralstonia solanacearum / Q000502:physiology; D011956:Receptors, Cell Surface / Q000378:metabolism*; D020156:Salicylic Acid / Q000378:metabolism; D015398:Signal Transduction; D014431:Tylenchoidea / Q000502:physiology*
D029681:Arabidopsis Proteins; C100975:PSK-alpha protein, plant; C515018:PSKR1 protein, Arabidopsis; D036361:Peptide Hormones; D010940:Plant Proteins; D011956:Receptors, Cell Surface; D020156:Salicylic Acid
giant cell; haustoria; oomycete; peptide signalling; root-knot nematode