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The impact of Spodoptera exigua herbivory on Meloidogyne incognita-induced root responses depends on the nematodes' life cycle stages.

ABSTRACT: Induced responses to above-ground and below-ground herbivores may interact via systemic signalling in plants. We investigated whether the impact of above-ground herbivory on root-knot nematode-induced responses depends on the nematode's life cycle stages. Tomato plants were infected with the nematode (Meloidogyne incognita) for 5, 15 or 30 days before receiving Spodoptera exigua caterpillars above-ground. We collected root materials after 24 h of caterpillar feeding. We investigated phytohormones and α-tomatine levels, and the expression of defence and glycoalkaloid metabolism (GAME) marker genes in tomato roots. Nematode infection alone increased the endogenous root levels of jasmonic acid (JA), salicylic acid (SA), abscisic acid (ABA), α-tomatine and the expression of the GLYCOALKALOID METABOLISM 1 (GAME1) gene mostly at 30 days post-nematode inoculation. Caterpillar feeding alone upregulated Lipoxygenase D and downregulated Basic-β-1-glucanase and GAME1 expression in roots. On nematode-infected plants, caterpillar feeding decreased JA levels, but it increased the expression of Leucine aminopeptidase A. The induction patterns of ABA and SA suggest that caterpillars cause cross-talk between the JA-signalling pathway and the SA and ABA pathways. Our results show that caterpillar feeding attenuated the induction of the JA pathway triggered by nematodes, mostly in the nematodes' reproduction stage. These results generate a better understanding of the molecular and chemical mechanisms underlying frequent nematode-plant-caterpillar interactions in natural and agricultural ecosystems.

SUBMITTER: Mbaluto CM

PROVIDER: S-EPMC7336558 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Plant root exudates affect root-knot nematodes egg hatch. Chemicals in root exudates can attract nematodes to the roots or result in repellence, motility inhibition or even death. However, until recently little was known about the relationship between tomato root exudates chemicals and root-knot nematodes. In this study, root exudates were extracted from three tomato rootstocks with varying levels of nematode resistance: Baliya (highly resistant, HR), RS2 (moderately resistant, MR) and L-402 (highly susceptible, T). The effects of the root exudates on Meloidogyne incognita (M. incognita) egg hatch, survival and chemotaxis of second-stage juveniles (J2) were explored. The composition of the root exudates was analysed by gas chromatography/mass spectrometry (GC/MS) prior to and following M. incognita inoculation. Four compounds in root exudates were selected for further analysis and their allopathic effect on M. incognita were investigated. Root exudates from each tomato rootstocks (HR, MR and T strains) suppressed M. incognita egg hatch and increased J2 mortality, with the highest rate being observed in the exudates from the HR plants. Exudate from HR variety also repelled M. incognita J2 while that of the susceptible plant, T, was demonstrated to be attractive. The relative amount of esters and phenol compounds in root exudates from HR and MR tomato rootstocks increased notably after inoculation. Four compounds, 2,6-Di-tert-butyl-p-cresol, L-ascorbyl 2,6-dipalmitate, dibutyl phthalate and dimethyl phthalate increased significantly after inoculation. The egg hatch of M. incognita was suppressed by each of the compound. L-ascorbyl 2,6-dipalmitate showed the most notable effect in a concentration-dependent manner. All four compounds were associated with increased J2 mortality. The greatest effect was observed with dimethyl phthalate at 2 mmol·L-1. Dibutyl phthalate was the only compound observed to repel M. incognita J2 with no effect being detected in the other compounds. Each of the four compounds were correlated with a reduction in disease index in the susceptible cultivar, T, and tomato seedlings irrigated with L-ascorbyl 2,6-dipalmitate at 2 mmol·L-1 showed the best resistance to M. incognita. Taken together, this study provided a valuable contribution to understanding the underlying mechanism of nematode resistance in tomato cultivars.

Project description:BackgroundSolanum torvum Sw is worldwide employed as rootstock for eggplant cultivation because of its vigour and resistance/tolerance to the most serious soil-borne diseases as bacterial, fungal wilts and root-knot nematodes. The little information on Solanum torvum (hereafter Torvum) resistance mechanisms, is mostly attributable to the lack of genomic tools (e.g. dedicated microarray) as well as to the paucity of database information limiting high-throughput expression studies in Torvum.ResultsAs a first step towards transcriptome profiling of Torvum inoculated with the nematode M. incognita, we built a Torvum 3' transcript catalogue. One-quarter of a 454 full run resulted in 205,591 quality-filtered reads. De novo assembly yielded 24,922 contigs and 11,875 singletons. Similarity searches of the S. torvum transcript tags catalogue produced 12,344 annotations. A 30,0000 features custom combimatrix chip was then designed and microarray hybridizations were conducted for both control and 14 dpi (day post inoculation) with Meloidogyne incognita-infected roots samples resulting in 390 differentially expressed genes (DEG). We also tested the chip with samples from the phylogenetically-related nematode-susceptible eggplant species Solanum melongena. An in-silico validation strategy was developed based on assessment of sequence similarity among Torvum probes and eggplant expressed sequences available in public repositories. GO term enrichment analyses with the 390 Torvum DEG revealed enhancement of several processes as chitin catabolism and sesquiterpenoids biosynthesis, while no GO term enrichment was found with eggplant DEG.The genes identified from S. torvum catalogue, bearing high similarity to known nematode resistance genes, were further investigated in view of their potential role in the nematode resistance mechanism.ConclusionsBy combining 454 pyrosequencing and microarray technology we were able to conduct a cost-effective global transcriptome profiling in a non-model species. In addition, the development of an in silico validation strategy allowed to further extend the use of the custom chip to a related species and to assess by comparison the expression of selected genes without major concerns of artifacts. The expression profiling of S. torvum responses to nematode infection points to sesquiterpenoids and chitinases as major effectors of nematode resistance. The availability of the long sequence tags in S. torvum catalogue will allow precise identification of active nematocide/nematostatic compounds and associated enzymes posing the basis for exploitation of these resistance mechanisms in other species.

Project description:Root-knot nematodes (RKNs) are a group of plant-parasitic nematodes that cause damage to various plant species and extensive economical losses. In this study, we performed integrated analysis of miRNA and mRNA expression data to explore the regulation of miRNA and mRNA in RKNs. In particular, we aimed to elucidate the mRNA targets of Meloidogyne incognita miRNAs and variations of the RKN transcriptome during five stages of its life cycle. Stage-wise RNA sequencing of M. incognita resulted in clean read numbers of 56,902,902, 50,762,456, 40,968,532, 47,309,223, and 51,730,234 for the egg, J2, J3, J4, and female stages, respectively. Overall, stage-dependent mRNA sequencing revealed that 17,423 genes were expressed in the transcriptome of M. incognita. The egg stage showed the maximum number of transcripts, and 12,803 gene transcripts were expressed in all stages. Functional Gene Ontology (GO) analysis resulted in three main GO classes: biological process, cellular components, and molecular function; the detected sequences were longer than sequences in the reference genome. Stage-wise selected fragments per kilobase of transcript per million mapped reads (FPKM) values of the top 10 stage-specific and common mRNAs were used to construct expression profiles, and 20 mRNAs were validated through quantitative real-time PCR (qRT-PCR). Next, we used three target prediction programs (miRanda, RNAhybrid, and PITA) to obtain 2431 potential target miRNA genes in RKNs, which regulate 8331 mRNAs. The predicted potential targets of miRNA were generally involved in cellular and metabolic processes, binding of molecules in the cell, membranes, and organelles. Stage-wise miRNA target analysis revealed that the egg stage contains heat shock proteins, transcriptional factors, and DNA repair proteins, whereas J2 includes DNA replication, heat shock, and ubiquitin-conjugating pathway-related proteins; the J3 and J4 stages are represented by the major sperm protein domain and translation-related proteins, respectively. In the female stage, we found proteins related to the maintenance of molybdopterin-binding domain-containing proteins and ubiquitin-mediated protein degradation. In total, 29 highly expressed stage-specific mRNA-targeting miRNAs were analyzed using qRT-PCR to validate the sequence analysis data. Overall, our findings provide new insights into the molecular mechanisms occurring at various developmental stages of the RKN life cycle, thus aiding in the identification of potential control strategies.

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The impact of Spodoptera exigua herbivory on Meloidogyne incognita-induced root responses depends on the nematodes' life cycle stages.

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