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Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot.

ABSTRACT: 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.

SUBMITTER: Gravot A

PROVIDER: S-EPMC5106811 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot.

Gravot Antoine A Richard Gautier G Lime Tanguy T Lemarié Séverine S Jubault Mélanie M Lariagon Christine C Lemoine Jocelyne J Vicente Jorge J Robert-Seilaniantz Alexandre A Holdsworth Michael J MJ Manzanares-Dauleux Maria J MJ

BMC plant biology 20161111 1

<h4>Background</h4>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.<h4>Results< ...[more]

PMID: 27835985

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Project description:BackgroundPlasmodiophora brassicae is the causal agent of clubroot disease of cruciferous plants and one of the biggest threats to the rapeseed (Brassica napus) and brassica vegetable industry worldwide.Disease symptomsIn the advanced stages of clubroot disease wilting, stunting, yellowing, and redness are visible in the shoots. However, the typical symptoms of the disease are the presence of club-shaped galls in the roots of susceptible hosts that block the absorption of water and nutrients.Host rangeMembers of the family Brassicaceae are the primary host of the pathogen, although some members of the family, such as Bunias orientalis, Coronopus squamatus, and Raphanus sativus, have been identified as being consistently resistant to P. brassicae isolates with variable virulence profile.TaxonomyClass: Phytomyxea; Order: Plasmodiophorales; Family: Plasmodiophoraceae; Genus: Plasmodiophora; Species: Plasmodiophora brassicae (Woronin, 1877).DistributionClubroot disease is spread worldwide, with reports from all continents except Antarctica. To date, clubroot disease has been reported in more than 80 countries.PathotypingBased on its virulence on different hosts, P. brassicae is classified into pathotypes or races. Five main pathotyping systems have been developed to understand the relationship between P. brassicae and its hosts. Nowadays, the Canadian clubroot differential is extensively used in Canada and has so far identified 36 different pathotypes based on the response of a set of 13 hosts.Effectors and resistanceAfter the identification and characterization of the clubroot pathogen SABATH-type methyltransferase PbBSMT, several other effectors have been characterized. However, no avirulence gene is known, hindering the functional characterization of the five intercellular nucleotide-binding (NB) site leucine-rich-repeat (LRR) receptors (NLRs) clubroot resistance genes validated to date.Important linkCanola Council of Canada is constantly updating information about clubroot and P. brassicae as part of their Canola Encyclopedia: https://www.canolacouncil.org/canola-encyclopedia/diseases/clubroot/.Phytosanitary categorizationPLADBR: EPPO A2 list; Annex designation 9E.

Dataset Information

Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot.

Publications

Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot.

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