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.
Highlights
Rice (Oryza sativa) is an important staple crop for a large part of the world population
We have reported that prior infection by the oomycete P. arrhenomanes consistently reduces the penetration rate and development of the root-knot nematode M. graminicola in rice roots, even under different infection and plant growth conditions (Verbeek et al, 2016)
To elucidate a potential mechanism behind this antagonism, we decided to investigate the levels of a set of plant hormones, namely JA, salicylic acid (SA), IAA—an important AUX—and abscisic acid (ABA), upon single and double inoculations, using root samples taken at two time points (11 and 13 days post germination, dpg) during the greenhouse experiment described in detail in Verbeek et al (2016)
Summary
Rice (Oryza sativa) is an important staple crop for a large part of the world population. Researchers use this plant as model organism for monocots. Jasmonates are lipid-derived signal molecules that play vital roles in diverse physiological processes, but have mostly been studied for their involvement in wounding responses, secondary metabolite biosynthesis, and defense. JA-Ile plays a vital role in jasmonate signaling by activating genes that are suppressed by transcriptional repressor proteins with a Jasmonate ZIM (JAZ) domain. Upon binding to JA-Ile, this complex directs ubiquitination and subsequent degradation of JAZ proteins via the proteasome (Pauwels and Goossens, 2011; Pieterse et al, 2012), leading to activation of JA-response genes. In Arabidopsis, the JA-responsive genes can be divided in two branches, where the MYC genes are associated with wound response and defense against insect herbivores, while other genes known as APETALA2/Ethylene Response Factor (AP2/ERF) genes are controlled by both JA and ET and are associated with enhanced resistance to necrotrophic pathogens (Zhu et al, 2011)
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