Jasmonate-Induced Defense Mechanisms in the Belowground Antagonistic Interaction Between Pythium arrhenomanes and Meloidogyne graminicola in Rice

Abstract

Next to their essential roles in plant growth and development, phytohormones play a central role in plant immunity against pathogens. In this study we studied the previously reported antagonism between the plant-pathogenic oomycete Pythium arrhenomanes and the root-knot nematode Meloidogyne graminicola, two root pathogens that co-occur in aerobic rice fields. In this manuscript, we investigated if the antagonism is related to imbalances in plant hormone levels, which could be involved in activation of plant defense. Hormone measurements and gene expression analyses showed that the jasmonate (JA) pathway is induced early upon P. arrhenomanes infection. Exogenous application of methyl-jasmonate (MeJA) on the plant confirmed that JA is needed for basal defense against both P. arrhenomanes and M. graminicola in rice. Whereas M. graminicola suppresses root JA levels to increase host susceptibility, Pythium inoculation boosts JA in a manner that prohibits JA repression by the nematode in double-inoculated plants. Exogenous MeJA supply phenocopied the defense-inducing capacity of Pythium against the root-knot nematode, whereas the antagonism was weakened in JA-insensitive mutants. Transcriptome analysis confirmed upregulation of JA biosynthesis and signaling genes upon P. arrhenomanes infection, and additionally revealed induction of genes involved in biosynthesis of diterpenoid phytoalexins, consistent with strong activation of the gene encoding the JA-inducible transcriptional regulator DITERPENOID PHYTOALEXIN FACTOR. Altogether, the here-reported data indicate an important role for JA-induced defense mechanisms in this antagonistic interaction. Next to that, our results provide evidence for induced expression of genes encoding ERF83, and related PR proteins, as well as auxin depletion in P. arrhenomanes infected rice roots, which potentially further contribute to the reduced nematode susceptibility seen in double-infected plants.

Chorismate mutase and isochorismatase, two potential effectors of the migratory nematode Hirschmanniella oryzae, increase host susceptibility by manipulating secondary metabolite content of rice

“…Transgenic lines deficient in OsCPS4 , a phytoalexin biosynthetic gene, showed increased susceptibility to rice blast fungus (Toyomasu et al, 2014). Also in nematodes it was shown that induction of DP biosynthesis increases resistance against nematodes (Verbeek et al, 2019). Some terpenoids might be involved in nematode resistance by accumulation in lesions near the infection site (Veech, 1982), so a reduced terpenoid content could influence susceptibility to nematodes.…”

Investigation of interactions between Meloidogyne javanica and three soil‐borne fungi against susceptible plant hosts

“…However, this hypothesis has evolved, suggesting diverse and more complicated mechanisms (e.g. physiological modifications, rhizosphere alternations) underlying these associations in different pathosystems (Back et al., 2002; Kyndt et al., 2017; Verbeek et al., 2019). Therefore, each plant‐fungus‐nematode association should be studied individually in order to assess the potential adverse effects on crops of interest, and estimate disease risk so as to develop effective management strategies.…”

“…Even more recently, Verbeek et al. (2019) revealed that Meloidogyne graminicola suppresses jasmonic acid (JA) levels in rice roots to increase host susceptibility, whereas Pythium arrhenomanes boosts JA in a manner that prohibits JA repression by the nematode, leading finally to decreased RKN infestation in dual‐inoculated plants. However, several authors have speculated that nematode penetration is increased in plant roots previously subjected to fungal pathogens or that feeding sites of sedentary endoparasitic nematodes are preferred infection sites for plant pathogenic fungi (Back et al., 2002).…”

A Phytochemical Perspective on Plant Defense Against Nematodes

“…For example, among cereals, maize (Zea mays) produces both diterpenoid (kauralexins and dolabralexins) and sesquiterpenoid (zealexins) phytoalexins (Block et al, 2019), while rice produces three different classes of diterpenoid phytoalexins: momilactones, phytocassanes, and oryzalexins (Yamane, 2013). All these terpenoids are involved in defense against fungal, bacterial, and/or insect pests and pathogens (Dillon et al, 1997;Lu et al, 2018;Pichersky and Raguso, 2018;Block et al, 2019), and they are inducible by treatment with resistance inducers that reduce susceptibility to nematodes (Yamane, 2013;Verbeek et al, 2019); it may thus prove fruitful to investigate their role in PPN resistance.…”