Transcriptome analysis reveals the high ribosomal inhibitory action of 1,4-naphthoquinone on Meloidogyne luci infective second-stage juveniles

Front Plant Sci. 2023 Jun 5:14:1191923. doi: 10.3389/fpls.2023.1191923. eCollection 2023.

Abstract

The root-knot nematode (RKN) Meloidogyne luci presents a threat to the production of several important crops. This nematode species was added to the European Plant Protection Organization Alert list in 2017. The scarce availability of efficient nematicides to control RKN and the phasing out of nematicides from the market have intensified the search for alternatives, such as phytochemicals with bionematicidal properties. The nematicidal activity of 1,4-naphthoquinone (1,4-NTQ) against M. luci has been demonstrated; however, knowledge of the potential mode(s) of action of this compound is still scarce. In this study, the transcriptome profile of M. luci second-stage juveniles (J2), the infective stage, in response to 1,4-NTQ exposure was determined by RNA-seq to identify genes and pathways that might be involved in 1,4-NTQ's mode(s) of action. Control treatments, consisting of nematodes exposed to Tween® 80 (1,4-NTQ solvent) and to water, were included in the analysis. A large set of differentially expressed genes (DEGs) was found among the three tested conditions, and a high number of downregulated genes were found between 1,4-NTQ treatment and water control, reflecting the inhibitory effect of this compound on M. luci, with a great impact on processes related to translation (ribosome pathway). Several other nematode gene networks and metabolic pathways affected by 1,4-NTQ were also identified, clarifying the possible mode of action of this promising bionematicide.

Keywords: Meloidogyne; bionematicide; naphthoquinone; plant-parasitic nematodes; transcriptome.

Grants and funding

This research was supported by the Portuguese Foundation for Science and Technology (FCT) through national funds and the co-funding by FEDER, PT2020, and COMPETE 2020 under the projects PTDC/ASP-PLA/29392/2017 (POCI-01-145-FEDER-029392), POCI-01-0145-FEDER-022184 (GenomePT), UIDB/04539/2020, UIDP/04539/2020, LA/P/0058/2020, UIDB/00102/2020, UIDP/00102/2020, UIDB/04004/2020, UIDP/04004/2020, and CEECIND/02082/2017 (IE), and by Instituto do Ambiente, Tecnologia e Vida.