WOX11-mediated cell size control in Arabidopsis attenuates growth and fecundity of endoparasitic cyst nematodes.

Arabidopsis thaliana Heterodera schachtii ROS WOX11 cell size cell wall plasticity cyst nematodes female fecundity syncytium hypertrophy

Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
14 Sep 2024
Historique:
received: 16 02 2024
accepted: 12 08 2024
medline: 15 9 2024
pubmed: 15 9 2024
entrez: 14 9 2024
Statut: aheadofprint

Résumé

Cyst nematodes establish permanent feeding structures called syncytia inside the host root vasculature, disrupting the flow of water and minerals. In response, plants form WOX11-mediated adventitious lateral roots at nematode infection sites. WOX11 adventitious lateral rooting modulates tolerance to nematode infections; however, whether this also benefits nematode parasitism remains unknown. Here, we report on bioassays using a 35S::WOX11-SRDX transcriptional repressor mutant to investigate whether WOX11 adventitious lateral rooting promotes syncytium development and thereby female growth and fecundity. Moreover, we chemically inhibited cellulose biosynthesis to verify if WOX11 directly modulates cell wall plasticity in syncytia. Finally, we performed histochemical analyses to test if WOX11 mediates syncytial cell wall plasticity via reactive oxygen species (ROS). Repression of WOX11-mediated transcription specifically enhanced the radial expansion of syncytial elements, increasing both syncytium size and female offspring. The enhanced syncytial hypertrophy observed in the 35S::WOX11-SRDX mutant could be phenocopied by chemical inhibition of cellulose biosynthesis and was associated with elevated levels of ROS at nematode infection sites. We, therefore, conclude that WOX11 restricts radial expansion of nematode-feeding structures and female growth and fecundity, likely by modulating ROS-mediated cell wall plasticity mechanisms. Remarkably, this novel role of WOX11 in plant cell size control is distinct from WOX11 adventitious lateral rooting underlying disease tolerance.

Identifiants

pubmed: 39276334
doi: 10.1111/tpj.16999
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Toegepaste en Technische Wetenschappen, NWO
ID : 14250
Organisme : Toegepaste en Technische Wetenschappen, NWO
ID : 17282
Organisme : Toegepaste en Technische Wetenschappen, NWO
ID : 18389
Organisme : Dutch Top Sector Horticulture & Starting Materials
ID : TU18152

Informations de copyright

© 2024 The Author(s). The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

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Auteurs

Nina Guarneri (N)

Laboratory of Nematology, Wageningen University & Research, Wageningen, 6708, PB, the Netherlands.

Jaap-Jan Willig (JJ)

Laboratory of Nematology, Wageningen University & Research, Wageningen, 6708, PB, the Netherlands.

Viola Willemsen (V)

Laboratory of Cell and Developmental Biology, Cluster of Plant Developmental Biology, Wageningen University & Research, Wageningen, 6708, PB, the Netherlands.

Aska Goverse (A)

Laboratory of Nematology, Wageningen University & Research, Wageningen, 6708, PB, the Netherlands.

Mark G Sterken (MG)

Laboratory of Nematology, Wageningen University & Research, Wageningen, 6708, PB, the Netherlands.

Pieter Nibbering (P)

Laboratory of Nematology, Wageningen University & Research, Wageningen, 6708, PB, the Netherlands.

José L Lozano Torres (JL)

Laboratory of Nematology, Wageningen University & Research, Wageningen, 6708, PB, the Netherlands.

Geert Smant (G)

Laboratory of Nematology, Wageningen University & Research, Wageningen, 6708, PB, the Netherlands.

Classifications MeSH