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(Homo)glutathione deficiency impairs root-knot nematode development in Medicago truncatula
- Source :
- PLoS Pathogens, Vol 8, Iss 1, p e1002471 (2012), PLoS Pathogens, PLoS Pathogens, Public Library of Science, 2012, 8 (1), pp.e1002471. ⟨10.1371/journal.ppat.1002471⟩, P L o S Pathogens, 8 (1, Plos Pathogens 1 (8), e1002471. (2012)
- Publication Year :
- 2012
- Publisher :
- Public Library of Science, 2012.
-
Abstract
- Root-knot nematodes (RKN) are obligatory plant parasitic worms that establish and maintain an intimate relationship with their host plants. During a compatible interaction, RKN induce the redifferentiation of root cells into multinucleate and hypertrophied giant cells essential for nematode growth and reproduction. These metabolically active feeding cells constitute the exclusive source of nutrients for the nematode. Detailed analysis of glutathione (GSH) and homoglutathione (hGSH) metabolism demonstrated the importance of these compounds for the success of nematode infection in Medicago truncatula. We reported quantification of GSH and hGSH and gene expression analysis showing that (h)GSH metabolism in neoformed gall organs differs from that in uninfected roots. Depletion of (h)GSH content impaired nematode egg mass formation and modified the sex ratio. In addition, gene expression and metabolomic analyses showed a substantial modification of starch and γ-aminobutyrate metabolism and of malate and glucose content in (h)GSH-depleted galls. Interestingly, these modifications did not occur in (h)GSH-depleted roots. These various results suggest that (h)GSH have a key role in the regulation of giant cell metabolism. The discovery of these specific plant regulatory elements could lead to the development of new pest management strategies against nematodes.<br />Author Summary Parasitic nematodes are microscopic worms that cause major diseases of plants, animals and humans. During compatible interactions, root-knot nematodes (RKN) induce the formation of galls in which redifferentiation of root cells into multinucleate and hypertrophied giant cells is essential for nematode growth and reproduction. The importance of glutathione (GSH), a major antioxidant molecule involved in plant development, in plant microbe interaction and in abiotic stress response, was analyzed during the plant-RKN interaction. Our analyses demonstrated that the gall development and functioning are characterized by an adapted GSH metabolism and that depletion of GSH content impairs nematode reproduction and modified sex ratio. This phenotype is linked to specific modifications of carbon metabolism which do not occur in uninfected roots indicating a peculiar metabolism of this neoformed organ. This first metabolomic analysis during the plant-RKN interaction highlights the regulatory role played by GSH in this pathogenic interaction and completes our vision of the role of GSH during plant-pathogen interactions. RKN sex ratio modification has previously been observed under unfavorable nematode feeding conditions suggesting that the GSH-redox system could be a general sensor of gall fitness in natural conditions.
- Subjects :
- 0106 biological sciences
Nematoda
[SDV]Life Sciences [q-bio]
Plant Science
Plant Roots
giant cell
nodule
gene expression
Medicago trunculata
RELATION PLANTE-MICROORGANISME
01 natural sciences
chemistry.chemical_compound
Gene Expression Regulation, Plant
Gall
nodosité
glutathion
lcsh:QH301-705.5
nématode
Regulation of gene expression
0303 health sciences
biology
Aminobutyrates
food and beverages
Starch
Sciences bio-médicales et agricoles
Glutathione
Medicago truncatula
Biochemistry
Medicago truncatula -- genetics -- metabolism -- parasitology
Research Article
lcsh:Immunologic diseases. Allergy
tripeptide
Immunology
Carbohydrate metabolism
légumineuse
Host-Parasite Interactions -- physiology
Microbiology
Host-Parasite Interactions
Aminobutyrates -- metabolism
03 medical and health sciences
Starch -- genetics -- metabolism
Virology
Botany
Genetics
medicine
Animals
Plant Diseases -- parasitology
Root-knot nematode
Biology
Molecular Biology
Plant Diseases
030304 developmental biology
Nematoda -- physiology
Glutathione -- analogs & derivatives -- biosynthesis -- genetics -- metabolism
Plant Pathology
medicine.disease
biology.organism_classification
Plant Roots -- genetics -- metabolism -- parasitology
Nematode
lcsh:Biology (General)
Nematode infection
chemistry
Parasitology
lcsh:RC581-607
010606 plant biology & botany
Subjects
Details
- Language :
- English
- ISSN :
- 15537366 and 15537374
- Database :
- OpenAIRE
- Journal :
- PLoS Pathogens, Vol 8, Iss 1, p e1002471 (2012), PLoS Pathogens, PLoS Pathogens, Public Library of Science, 2012, 8 (1), pp.e1002471. ⟨10.1371/journal.ppat.1002471⟩, P L o S Pathogens, 8 (1, Plos Pathogens 1 (8), e1002471. (2012)
- Accession number :
- edsair.doi.dedup.....2659a6d60b11774f16db7c517ae0bdbf