Leaf herbivory counteracts nematode-triggered repression of jasmonate-related defenses in tomato roots

17 páginas, 8 figuras

Shoot herbivores may influence the communities of herbivores associated with the roots via inducible defenses. However, the molecular mechanisms and hormonal signaling underpinning the systemic impact of leaf herbivory on root-induced responses against nematodes remain poorly understood. By using tomato (Solanum lycopersicum) as a model plant, we explored the impact of leaf herbivory by Manduca sexta on the performance of the root knot nematode Meloidogyne incognita. By performing glasshouse bioassays, we found that leaf herbivory reduced M. incognita performance in the roots. By analyzing the root expression profile of a set of oxylipin-related marker genes and jasmonate root content, we show that leaf herbivory systemically activates the 13-Lipoxigenase (LOX) and 9-LOX branches of the oxylipin pathway in roots and counteracts the M. incognita-triggered repression of the 13-LOX branch. By using untargeted metabolomics, we also found that leaf herbivory counteracts the M. incognita-mediated repression of putative root chemical defenses. To explore the signaling involved in this shoot-to-root interaction, we performed glasshouse bioassays with grafted plants compromised in jasmonate synthesis or perception, specifically in their shoots. We demonstrated the importance of an intact shoot jasmonate perception, whereas having an intact jasmonate biosynthesis pathway was not essential for this shoot-to-root interaction. Our results highlight the impact of leaf herbivory on the ability of M. incognita to manipulate root defenses and point to an important role for the jasmonate signaling pathway in shoot-to-root signaling.

This research was supported by the German Research Foundation (DFG–FZT 118, 202548816), by the program for attracting talent to Salamanca from Fundacio´n Salamanca Ciudad de Cultura y Saberes and Ayuntamiento de Salamanca (to A.M.M.), by the program to support junior researchers to obtain third-party funding from FriedrichSchiller-Universita¨t Jena (DRM/2015-02, to A.M.M.) y the Deutscher Akademischer Austauschdienst (DAAD 91607343, to C.M.M); by Junta de Castilla y León and European Union (ERDF “Europe drives our growth”; CLU-2019-05 – IRNASA/CSIC Unit of Excellence); and the research network RED2018-102407-T from the Spanish Ministry of Science and Innovation and Feder funds.

Peer reviewed