The root-knot nematode effector MiPFN3 disrupts plant actin filaments and promotes parasitism

Abstract

Root-knot nematodes secrete effectors that manipulate their host plant cells so that the nematode can successfully establish feeding sites and complete its lifecycle. The root-knot nematode feeding structures, their “giant cells,” undergo extensive cytoskeletal remodeling. Previous cytological studies have shown the cytoplasmic actin within the feeding sites looks diffuse. In an effort to study root-knot nematode effectors that are involved in giant cell organogenesis, we have identified a nematode effector called MiPFN3 (Meloidogyne incognita Profilin 3). MiPFN3 is transcriptionally up-regulated in the juvenile stage of the nematode. In situ hybridization experiments showed that MiPFN3 transcribed in the nematode subventral glands, where it can be secreted by the nematode stylet into the plant. Moreover, Arabidopsis plants that heterologously expressed MiPFN3 were more susceptible to root-knot nematodes, indicating that MiPFN3 promotes nematode parasitism. Since profilin proteins can bind and sequester actin monomers, we investigated the function of MiPFN3 in relation to actin. Our results show that MiPFN3 suppressed the aberrant plant growth phenotype caused by the misexpression of reproductive actin (AtACT1) in transgenic plants. In addition, it disrupted actin polymerization in an in vitro assay, and it reduced the filamentous actin network when expressed in Arabidopsis protoplasts. Over a decade ago, cytological studies showed that the cytoplasmic actin within nematode giant cells looked fragmented. Here we provide the first evidence that the nematode is secreting an effector that has significant, direct effects on the plant’s actin cytoskeleton.

Large-Scale Identification and Characterization of Heterodera avenae Putative Effectors Suppressing or Inducing Cell Death in Nicotiana benthamiana

“…Actin reorganization is crucial for the development and expansion of nematode feeding sites. When Mi131, a protein from M. incognita that bears a profilin domain, was expressed in protoplasts in which the actin cytoskeleton had been labeled with GFP, the actin cytoskeleton appeared fragmented ( Leelarasamee, 2015 ). Profilin from the protozoan parasite Toxoplasma gondii plays a role in motility and serves as a microbial ligand that is recognized by the host innate immune system, functioning like bacterial flagellin ( Plattner et al, 2008 ).…”

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

“…Some other effector proteins can also bind actin monomers to manipulate plant actin in conjunction with the enhancement of the expression of the genes encoding endogenous actin-depolymerizing factor (ADF), as described for MiPFN3 in M. incognita by Leelarasamee et al (2018). Their results suggested that diminishing actin network density was important to facilitate nematode feeding.…”

Analyses of the Root-Knot Nematode (Meloidogyne graminicola) Transcriptome during Host Infection Highlight Specific Gene Expression Profiling in Resistant Rice Plants

“… Schematic representation of the gene expression patterns of 38 Meloidogyne graminicola genes encoding candidate effectors or homologs of Meloidogyne effectors [ 10 , 11 , 12 , 13 , 14 , 15 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 ]. Each row represents a gene and each column represents a stage of nematode development (J2: pre-parasitic J2s, Nip: in susceptible rice plants, Tog: in resistant rice plants) either at 2, 4 or 8 dpi.…”