A novel nematode effector suppresses plant immunity by activating host reactive oxygen species‐scavenging system

Abstract

Summary Evidence is emerging that plant‐parasitic nematodes can secrete effectors to interfere with the host immune response, but it remains unknown how these effectors can conquer host immune responses. Here, we depict a novel effector, MjTTL5, that could suppress plant immune response.Immunolocalization and transcriptional analyses showed that MjTTL5 is expressed specifically within the subventral gland of Meloidogyne javanica and up‐regulated in the early parasitic stage of the nematode. Transgenic Arabidopsis lines expressing MjTTL5 were significantly more susceptible to M. javanica infection than wild‐type plants, and vice versa, in planta silencing of MjTTL5 substantially increased plant resistance to M. javanica.Yeast two‐hybrid, coimmunoprecipitation and bimolecular fluorescent complementation assays showed that MjTTL5 interacts specifically with Arabidopsis ferredoxin : thioredoxin reductase catalytic subunit (AtFTRc), a key component of host antioxidant system. The expression of AtFTRc is induced by the infection of M. javanica. Interaction between AtFTRc and MjTTL could drastically increase host reactive oxygen species‐scavenging activity, and result in suppression of plant basal defenses and attenuation of host resistance to the nematode infection.Our results demonstrate that the host ferredoxin : thioredoxin system can be exploited cunningly by M. javanica, revealing a novel mechanism utilized by plant–parasitic nematodes to subjugate plant innate immunity and thereby promoting parasitism.

The Ralstonia solanacearum type III effector RipAY targets plant redox regulators to suppress immune responses

“…Indeed, the victorin toxin from the fungus Cochliobolus victoriae takes advantage of the guarding of plant TRXs by NB‐LRR proteins to induce cell death in plants, which promotes disease development (Lorang et al ., ; Sweat and Wolpert, ). Recently, an effector from the plant‐parasitic nematode Meloidogyne javanica has been found to manipulate the ferredoxin–thioredoxin system in root plastids, which activates ROS scavenging and suppresses immune responses, enhancing susceptibility to the nematode (Lin et al ., ). Arabidopsis TRX‐h5 and TRX‐h3 have also been found to interact with an effector from the plant‐pathogenic oomycete Hyaloperonospora arabidopsidis (Wessling et al ., ).…”

RNA‐Seq identification of candidate defense genes targeted by endophytic Bacillus cereus‐mediated induced systemic resistance against Meloidogyne incognita in tomato

“…Recently, evidence emerged that PPNs can interfere with the host PTI response by secreting effector proteins. Mi‐CRT and Misp12 from M. incognita and MjTTL5 from M. javanica are effectors in PPNs that suppress PTI . The study of plant defenses against nematodes has concentrated on disease resistance proteins and effector‐triggered immunity (ETI) .…”

“…Meanwhile, the level of induced resistance was shown to be further enhanced when both ISR and SAR are activated simultaneously in Arabidopsis . Plant defense responses include resistance against infection by pathogens and parasites, which is commonly recognized as a pathogen‐associated molecular pattern (PAMP), leading to pattern‐triggered immunity (PTI) . Subsequently, many events are induced: activation of the mitogen‐activated protein kinase (MAPK) signaling cascade, callose deposition, bursts of reactive oxygen species, and rapid changes in gene expression .…”

Plant-parasitic nematodes: towards understanding molecular players in stress responses

“…This interaction is correlated with ROS scavenging and plant susceptibility against PPNs. Because ROS, particularly H 2 O 2 , are signalling molecules in plant immunity, their suppression is associated with the attenuation of host resistance to nematode infection (Lin et al , 2016). Notably, both PPN effectors (annexin-like and transthyretin-like effectors) are derived from ancient protein families that are conserved in the plant and animal kingdoms, with their functions often associated with oxidative stress (Richardson and Cody, 2009; Clark et al , 2010; Lauritzen et al , 2015).…”