A novel Meloidogyne incognita chorismate mutase effector suppresses plant immunity by manipulating the salicylic acid pathway and functions mainly during the early stages of nematode parasitism

Abstract

Meloidogyne incognita is the most economically important plant‐parasitic nematode. Meloidogyne incognita manipulates plant cell development and metabolism by injecting effectors from the oesophageal glands into the plant host. Chorismate mutase (CM) is one such effector that may contribute to successful parasitism by M. incognita. This investigation identified and functionally characterized a novel CM effector, Mi‐CM‐3, which is more similar to CMs from bacteria than from other phytoparasitic nematodes. Spatial and temporal expression assays showed Mi‐cm‐3 mRNA accumulates specifically in the subventral oesophageal glands and transcription is up‐regulated during the early parasitic stages of the nematode. In planta gene silencing of Mi‐cm‐3 attenuated nematode parasitism. In addition, Mi‐cm‐3 could fully restore the full virulence phenotype of the pathogenic bacterium Xanthomonas oryzae pv. oryzae by complementation when it was introduced into a mutant strain carrying a deletion in the CM gene. Transient expression of Mi‐CM‐3 caused a reduction in levels of salicylic acid (SA) and mRNA of gene PR1 in Nicotiana benthamiana in response to oomycete pathogen Phytophthora capsici infection, while confocal observations showed that Mi‐CM‐3 was localized within the cytoplasm and the nucleus, but not the plastids, of transfected N. benthamiana leaf cells. Constitutive expression of Mi‐CM‐3 in N. benthamiana plants inhibited root growth and increased susceptibility to M. incognita infection. These results provide direct experimental evidence to show that Mi‐CM‐3 may play an important role in suppressing plant immunity by regulating the SA pathway during the early parasitic stage of M. incognita so as to promote nematode parasitism.

Salicylic Acid Biosynthesis in Plants

“…Several plant-parasitic nematode species also produce isochorismatases (Bauters et al, 2014). Plant-parasitic nematodes also secrete CM (Haegeman et al, 2013), that can divert chorismate away from the ICS pathway, thus limiting SA accumulation (Wang et al, 2018). In maize, the fungus Ustilago maydis also secretes CM (Djamei et al, 2011).…”

Plant defense responses in monocotyledonous and dicotyledonous host plants during root-knot nematode infection

“…This protein was suggested to be involved in the downregulation of SA-and JA-dependent defense response genes to enhance M. incognita parasitism during the mature stages of the nematode life cycle (Xie et al 2016). On the other hand, Wang et al (2018) characterized a novel chorismate mutase from M. incognita, Mi-CM3, which regulated the SA pathway in such a way that enhanced nematode parasitism. Mi-CM3 disrupts SA biosynthesis and SAmediated defense in the plant tissues in which this gene is expressed.The presence of a chorismate mutase was also reported in M. javanica species (MjCM-1), and the authors assumed that this protein has the potential to be a multifunctional enzyme responsible for promoting nematode pathogenicity (Doyle and Lambert 2003).…”

Phytoparasitic Nematode Control of Plant Hormone Pathways

“…Similar genes have been identified in plant-parasitic nematodes (see Table 1). Wang et al (2018) demonstrated that transient expression of an M. incognita chorismate mutase effector in Nicotiana benthamiana causes a decline in SA levels and larger…”