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The impact of root infection by the nematode Meloidogyne incognita on leaf anti-herbivore defenses and plant resistance to the caterpillar Spodoptera exigua is modulated by the nematode infection cycle., Studies on plant-mediated interactions between root parasitic nematodes and aboveground herbivores are rapidly increasing. However, outcomes for the interacting organisms vary, and the mechanisms involved remain ambiguous. We hypothesized that the impact of root infection by the root-knot nematode Meloidogyne incognita on the performance of the aboveground caterpillar Spodoptera exigua is modulated by the nematode’s infection cycle. We challenged root-knot nematode-infected tomato plants with caterpillars when the nematode’s infection cycle was at the invasion, galling, and reproduction stages. We found that M. incognita root infection enhanced S. exigua performance during the galling stage, while it did not affect the caterpillar’s performance at the invasion and reproduction stages. Molecular and chemical analyses performed at the different stages of the nematode infection cycle revealed that M. incognita root infection systemically affected the jasmonic acid-, salicylic acid-, and abscisic acid-related responses, as well as the changes in the leaf metabolome triggered during S. exigua feeding. The M. incognita-induced leaf responses varied over the nematode’s root infection cycle. These findings suggest that specific leaf responses triggered systemically by the nematode at its different life-cycle stages underlie the differential impact of M. incognita on plant resistance against the caterpillar S. exigua.

18 páginas, 7 figuras, 2 tablas, Studies on plant-mediated interactions between root parasitic nematodes and aboveground herbivores are rapidly increasing. However, the outcomes for the interacting organisms vary, and the mechanisms involved remain ambiguous. We hypothesized that the impact of root infection by the root-knot nematode Meloidogyne incognita on the performance of the aboveground caterpillar Spodoptera exigua is modulated by the nematode's infection cycle. We challenged root-knot nematode infected tomato plants with caterpillars when the nematode's infection cycle was either at the invasion, galling, or reproduction stage. We found that M. incognita root infection enhanced S. exigua performance during the galling stage, while it did not affect the caterpilar's performance at the invasion and reproduction stages. Molecular and chemical analyses performed at the different stages of the nematode infection cycle revealed that M. incognita root infection systemically affected the jasmonic acid-, salicylic acid- and abscisic acid-related responses, as well as changes in the leaf metabolome during S. exigua feeding. The M. incognita induced leaf responses significantly varied over the nematode's root infection cycle. These findings suggest that specific leaf responses triggered systemically by the nematode at its different life-cycle stages underlie the differential impact of M. incognita on plant resistance against the caterpillar S. exigua., All authors gratefully acknowledge the support of the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig funded by the German Research Foundation (DFG-FZT 118, 202548816). CMM acknowledges the Deutscher Akademischer Austauschdienst (DAAD) for a doctoral research grant (research grant No: 91607343). AMM acknowledges funding from the program for attracting talent to Salamanca from the Fundación Salamanca Ciudad de Cultura y Saberes and Ayuntamiento de Salamanca; the program to support junior researchers to obtain thirdparty funding from Friedrich-Schiller-Universitat Jena (DRM/2015-02); 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