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The root-knot nematode effector MiPFN3 disrupts plant actin filaments and promotes parasitism
PLOS Pathogens plospathogens/article?id=10. 1371/journal.ppat.1006947

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  • Natthanon Leelarasamee,
  • Lei Zhang,
  • Cynthia Gleason 
    • PLOS
    • Published: March 15, 2018
    • journal.ppat.1006947

    • 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 incognitaProfilin 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.

      Author summary

      Root-knot nematodes are microscopic plant pests that infect plant roots and significantly reduce yields of many crop plants. The nematodes enter the plant roots and modify plant cells into complex, multinuclear feeding sites called giant cells. The formation and maintenance of giant cells is critical to nematode survival. During giant cell organogenesis, the progenitor plant cells undergo many morphological changes, including a re-organization of the cytoplasmic actin cytoskeleton. As a result, the giant cell cytoplasmic actin appears fragmented and disorganized. Plant cells can regulate their actin filament assembly, in part, through the expression of actin binding proteins such as profilins. Here we show that infectious nematode juveniles express a profilin called MiPFN3. Expression of MiPFN3 in Arabidopsis plants made the plants more susceptible to root-knot nematodes, indicating that MiPFN3 acts as an effector that aids parasitism. We show evidence that the expression MiPFN3 in plant cells causes the fragmentation of plant actin filaments. The work here demonstrates that nematode effector MiPFN3 can directly affect plant actin filaments, whose reorganization is necessary for giant cell formation.


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