Root infection by the nematode Meloidogyne incognita modulates leaf antiherbivore defenses and plant resistance to Spodoptera exigua

Author:

Mbaluto Crispus M12ORCID,Vergara Fredd1,van Dam Nicole M12ORCID,Martínez-Medina Ainhoa123ORCID

Affiliation:

1. Molecular Interaction Ecology, German Center for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig; PuschStraße 4, 04103, Leipzig, Germany

2. Institute of Biodiversity, Friedrich-Schiller-Universität-Jena; DornburgerStraße 159, 07743 Jena, Germany

3. Plant-Microorganism Interaction, Institute of Natural Resources and Agrobiology of Salamanca (IRNASA-CSIC), Cordel de Merinas, 40, 37008, Salamanca, Spain

Abstract

Abstract 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.

Funder

German Research Foundation

Deutscher Akademischer Austauschdienst

Fundación Salamanca Ciudad de Cultura y Saberes and Ayuntamiento de Salamanca

Friedrich-Schiller-Universitat Jena

Junta de Castilla y León and European Union

Spanish Ministry of Science and Innovation and Feder funds

Publisher

Oxford University Press (OUP)

Subject

Plant Science,Physiology

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