Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot.
The induction of alcohol fermentation in roots is a plant adaptive response to flooding stress and oxygen deprivation. Available transcriptomic data suggest that fermentation-related genes are also frequently induced in roots infected with gall forming pathogens, but the biological significance of this induction is unclear. In this study, we addressed the role of hypoxia responses in Arabidopsis roots during infection by the clubroot agent Plasmodiophora brassicae.



The hypoxia-related gene markers PYRUVATE DECARBOXYLASE 1 (PDC1), PYRUVATE DECARBOXYLASE 2 (PDC2) and ALCOHOL DEHYDROGENASE 1 (ADH1) were induced during secondary infection by two isolates of P. brassicae, eH and e2. PDC2 was highly induced as soon as 7 days post inoculation (dpi), i.e., before the development of gall symptoms, and GUS staining revealed that ADH1 induction was localised in infected cortical cells of root galls at 21 dpi. Clubroot symptoms were significantly milder in the pdc1 and pdc2 mutants compared with Col-0, but a null T-DNA insertional mutation of ADH1 did not affect clubroot susceptibility. The Arg/N-end rule pathway of ubiquitin-mediated proteolysis controls oxygen sensing in plants. Mutants of components of this pathway, ate1 ate2 and prt6, that both exhibit constitutive hypoxia responses, showed enhanced clubroot symptoms. In contrast, gall development was reduced in quintuple and sextuple mutants where the activity of all oxygen-sensing Group VII Ethylene Response Factor transcription factors (ERFVIIs) is absent (erfVII and prt6 erfVII).



Our data demonstrate that the induction of PDC1 and PDC2 during the secondary infection of roots by P. brassicae contributes positively to clubroot development, and that this is controlled by oxygen-sensing through ERFVIIs. The absence of any major role of ADH1 in symptom development may also suggest that PDC activity could contribute to the formation of galls through the activation of a PDH bypass.
IGEPP, AGROCAMPUS OUEST, INRA, Université de Rennes 1, 35650, Le Rheu, France. antoine.gravot@univ-rennes1.fr.
Antoine
A
Gravot
IGEPP, AGROCAMPUS OUEST, INRA, Université de Rennes 1, 35650, Le Rheu, France.
Gautier
G
Richard
IGEPP, AGROCAMPUS OUEST, INRA, Université de Rennes 1, 35650, Le Rheu, France.
Tanguy
T
Lime
IGEPP, AGROCAMPUS OUEST, INRA, Université de Rennes 1, 35650, Le Rheu, France.
Séverine
S
Lemarié
IGEPP, AGROCAMPUS OUEST, INRA, Université de Rennes 1, 35650, Le Rheu, France.
Mélanie
M
Jubault
IGEPP, AGROCAMPUS OUEST, INRA, Université de Rennes 1, 35650, Le Rheu, France.
Christine
C
Lariagon
IGEPP, AGROCAMPUS OUEST, INRA, Université de Rennes 1, 35650, Le Rheu, France.
Jocelyne
J
Lemoine
Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough, LE12 5RD, UK.
Jorge
J
Vicente
IGEPP, AGROCAMPUS OUEST, INRA, Université de Rennes 1, 35650, Le Rheu, France.
Alexandre
A
Robert-Seilaniantz
Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough, LE12 5RD, UK.
Michael J
MJ
Holdsworth
IGEPP, AGROCAMPUS OUEST, INRA, Université de Rennes 1, 35650, Le Rheu, France.
Maria J
MJ
Manzanares-Dauleux
D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism* / Q000469:parasitology*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D010935:Plant Diseases / Q000469:parasitology; D018517:Plant Roots / Q000235:genetics / Q000378:metabolism / Q000469:parasitology; D056909:Plasmodiophorida / Q000502:physiology*
D029681:Arabidopsis Proteins
ADH1; Arabidopsis; Clubroot; ERFVII; Ethanol fermentation; Hypoxia; N-end rule pathway; PDC2; Plant gall disease; Plasmodiophora