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

Kazuki Sato,Takahiro Bino,Shahid Siddique,Taketo Uehara,Yasunori Ichihashi,Katsushi Yamaguchi,Pamela Gan,Florian M W Grundler,Shuji Shigenobu,Yasuhiro Kadota,Yuko Sasaki-Sekimoto,Ken Shirasu,Hiroyuki Ohta,Rochus B Franke,Takamasa Suzuki,Noriko Maki,Julia Holbein

doi:10.3389/fpls.2021.680151

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.

Highlights

Plant-parasitic nematodes (PPNs) infect a broad range of commercially important crop families such as the Solanaceae, Fabaceae, Malvaceae, Amaranthaceae, and Poaceae
These results suggest that S. torvum rapidly induces defense responses against A2-O, which inhibits the maturation of A2O and gall formation
We found that the genes that are highly expressed after infection with A2-O in Cluster 8 and 9 include (1) defense-related genes encoding chitinase, β-1,3-glucanase, and serine protease inhibitor, (2) sesquiterpene synthase, (3) fatty acid desaturase 2 (FAD2), (4) ferulic acid 5-hydroxylase (F5H) which is involved in lignin biosynthesis, (5) berberine bridge enzyme (BBE)-like protein, which is involved in oxidation of cinnamyl alcohol (Figure 5B)

Summary

Introduction

Plant-parasitic nematodes (PPNs) infect a broad range of commercially important crop families such as the Solanaceae (tomato, potato, pepper), Fabaceae (soybean, lucerne, lentils), Malvaceae (cotton), Amaranthaceae (sugar beet), and Poaceae The most economically important group of PPNs are sedentary endoparasites, including root-knot nematodes (RKNs) and cyst nematodes (CNs) (Palomares-Rius et al, 2017). Sedentary endoparasites induce the formation of permanent feeding cells that provide specialized nutrient sources for nematodes (Bartlem et al, 2014; Siddique and Grundler, 2018; Smant et al, 2018). Infective second-stage juveniles (J2s) of RKNs (Meloidogyne spp.) predominantly invade near the root tip and migrate intercellularly toward the apical meristematic region without crossing the endodermis, making a U-turn to enter the vascular cylinder where they induce several giant cells as a feeding site by stimulating the redifferentiation of root cells into multinucleate giant cells by repeated nuclear divisions without cytoplasmic division. A CN female produces hundreds of eggs and its body forms a cyst that can protect the eggs for many years in the soil (Wyss and Zunke, 1986; Bohlmann and Sobczak, 2014; Bohlmann, 2015)

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Conclusion