Root architecture plasticity in response to endoparasitic cyst nematodes is mediated by damage signaling

• Published in: The New phytologist Vol. 237; no. 3; pp. 807 - 822
• Main Authors: Guarneri, Nina, Willig, Jaap‐Jan, Sterken, Mark G., Zhou, Wenkun, Hasan, M. Shamim, Sharon, Letia, Grundler, Florian M. W., Willemsen, Viola, Goverse, Aska, Smant, Geert, Lozano‐Torres, Jose L.
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 01.02.2023; John Wiley and Sons Inc
• Subjects: Animals; Arabidopsis; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; auxin; Auxins; Biosynthesis; biotic stress; cyst nematodes; Damage; Density; Endoparasites; ERF109; Heterodera schachtii; Indoleacetic Acids - metabolism; Infections; jasmonates; Jasmonic acid; Molecular modelling; Mutation; nematode infections; Nematode Infections - metabolism; Nematodes; Plant Diseases - parasitology; Plant roots; Plant Roots - metabolism; Plants; Plastic properties; Plasticity; root architecture; root plasticity; Roots; Tylenchoidea - physiology; Arabidopsis thaliana; root plasticity; damage; root architecture; ERF109; auxin; jasmonates; Heterodera schachtii
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.18570

Summary Plant root architecture plasticity in response to biotic stresses has not been thoroughly investigated. Infection by endoparasitic cyst nematodes induces root architectural changes that involve the formation of secondary roots at infection sites. However, the molecular mechanisms regulating secondary root formation in response to cyst nematode infection remain largely unknown. We first assessed whether secondary roots form in a nematode density‐dependent manner by challenging wild‐type Arabidopsis plants with increasing numbers of cyst nematodes (Heterodera schachtii). Next, using jasmonate‐related reporter lines and knockout mutants, we tested whether tissue damage by nematodes triggers jasmonate‐dependent secondary root formation. Finally, we verified whether damage‐induced secondary root formation depends on local auxin biosynthesis at nematode infection sites. Intracellular host invasion by H. schachtii triggers a transient local increase in jasmonates, which activates the expression of ERF109 in a COI1‐dependent manner. Knockout mutations in COI1 and ERF109 disrupt the nematode density‐dependent increase in secondary roots observed in wild‐type plants. Furthermore, ERF109 regulates secondary root formation upon H. schachtii infection via local auxin biosynthesis. Host invasion by H. schachtii triggers secondary root formation via the damage‐induced jasmonate‐dependent ERF109 pathway. This points at a novel mechanism underlying plant root plasticity in response to biotic stress.