Transcriptomic Analysis of Resistant and Susceptible Responses in a New Model Root-Knot Nematode Infection System Using Solanum torvum and Meloidogyne arenaria

Abstract

Root-knot nematodes (RKNs) are among the most devastating pests in agriculture. Solanum torvum Sw. (Turkey berry) has been used as a rootstock for eggplant (aubergine) cultivation because of its resistance to RKNs, including Meloidogyne incognita and M. arenaria. We previously found that a pathotype of M. arenaria, A2-J, is able to infect and propagate in S. torvum. In vitro infection assays showed that S. torvum induced the accumulation of brown pigments during avirulent pathotype A2-O infection, but not during virulent A2-J infection. This experimental system is advantageous because resistant and susceptible responses can be distinguished within a few days, and because a single plant genome can yield information about both resistant and susceptible responses. Comparative RNA-sequencing analysis of S. torvum inoculated with A2-J and A2-O at early stages of infection was used to parse the specific resistance and susceptible responses. Infection with A2-J did not induce statistically significant changes in gene expression within one day post-inoculation (DPI), but afterward, A2-J specifically induced the expression of chalcone synthase, spermidine synthase, and genes related to cell wall modification and transmembrane transport. Infection with A2-O rapidly induced the expression of genes encoding class III peroxidases, sesquiterpene synthases, and fatty acid desaturases at 1 DPI, followed by genes involved in defense, hormone signaling, and the biosynthesis of lignin at 3 DPI. Both isolates induced the expression of suberin biosynthetic genes, which may be triggered by wounding during nematode infection. Histochemical analysis revealed that A2-O, but not A2-J, induced lignin accumulation at the root tip, suggesting that physical reinforcement of cell walls with lignin is an important defense response against nematodes. The S. torvum-RKN system can provide a molecular basis for understanding plant-nematode interactions.

Profiling ofZea maysL. proteome at early stages of compatible interactions withMeloidogyne arenariaindicates changes in signaling, oxidative stress responses, and S-adenosylmethionine biosynthesis

“…The major proteins annotated to defense response, response to oxidative stress, and lipid oxidation processes were peroxidases, alpha-dioxygenase, allene oxide synthesis, lipoxygenase, and benzoate O-methyltransferase (Supplementary Tables S3 and S4). Interestingly, the expression of genes encoding class III peroxidases was induced at 24 hpi, followed by the induction of the expression of genes involved in defense response at 3 dpi during compatible interactions between M. arenaria and S. torvum (Sato et al 2021), which partially overlaps with results observed in this study. On the other hand, we previously reported downregulation of gene encoding peroxidase in all analyzed time points (24 hpi, 3 dpi, and 7 dpi) in maize response to M. arenaria infection.…”

“…incognita infection (Shukla et al 2018). Induction of genes related to cell wall modifications was also observed during Solanum torvum's response to M. arenaria infection (Sato et al 2021). These data overlap with results described in this study, where changes in the accumulation level of proteins related to cell wall modifications were observed at both time points.…”

RNA-Seq of Cyst Nematode Infestation of Potato (Solanum tuberosum L.): A Comparative Transcriptome Analysis of Resistant and Susceptible Cultivars

“…Another study suggested that physical reinforcement of cell walls with lignin is an important defense response against nematodes. The Solanum torvum-root-knot nematode system can provide a molecular basis for understanding plant-nematode interactions [40]. In S. torvum, a resistant root stock for eggplant and root-knot nematode interactions, infestation by an avirulent pathotype of Meloidogyne arenaria induced the expression of several genes such as class III peroxidases, fatty acid desaturases, sesquiterpene synthases, and genes involved in defense, hormone signaling, biosynthesis of lignin, etc., which contribute to resistance.…”

Understanding Molecular Plant–Nematode Interactions to Develop Alternative Approaches for Nematode Control

“…Although there are a good number of resistant genotypes, an urgent need is apparent for more ones to reduce PPN losses. Moreover, the majority of plant resistance genes used are effective against only the above-mentioned sedentary nematode category [30,33,42]. Hence, introgression of R-genes to confer nematode resistance to susceptible plants via classical genetic breeding can offer potent steps change in crop productivity [43][44][45].…”