The Cyst Nematode Effector Protein 10A07 Targets and Recruits Host Posttranslational Machinery to Mediate Its Nuclear Trafficking and to Promote Parasitism in Arabidopsis

Abstract

Plant-parasitic cyst nematodes synthesize and secrete effector proteins that are essential for parasitism. One such protein is the 10A07 effector from the sugar beet cyst nematode, Heterodera schachtii, which is exclusively expressed in the nematode dorsal gland cell during all nematode parasitic stages. Overexpression of H. schachtii 10A07 in Arabidopsis thaliana produced a hypersusceptible phenotype in response to H. schachtii infection along with developmental changes reminiscent of auxin effects. The 10A07 protein physically associates with a plant kinase and the IAA16 transcription factor in the cytoplasm and nucleus, respectively. The interacting plant kinase (IPK) phosphorylates 10A07 at Ser-144 and Ser-231 and mediates its trafficking from the cytoplasm to the nucleus. Translocation to the nucleus is phosphorylation dependent since substitution of Ser-144 and Ser-231 by alanine resulted in exclusive cytoplasmic accumulation of 10A07. IPK and IAA16 are highly upregulated in the nematode-induced syncytium (feeding cells), and deliberate manipulations of their expression significantly alter plant susceptibility to H. schachtii in an additive fashion. An inactive variant of IPK functioned antagonistically to the wild-type IPK and caused a dominant-negative phenotype of reduced plant susceptibility. Thus, exploitation of host processes to the advantage of the parasites is one mechanism by which cyst nematodes promote parasitism of host plants.

Plant-Pathogen Effectors: Cellular Probes Interfering with Plant Defenses in Spatial and Temporal Manners

“…Nematode effectors also interfere with host transcription. The 10A07 effector from the sugar beet nematode H. schachtii is phosphorylated by the plant kinase IPK, facilitating its nuclear localization and interaction with the auxin-responsive transcription factor INDOLE-3-ACETIC ACIDINDUCIBLE16(IAA16) (46). Thus, 10A07 interferes with auxin signaling by its interaction with IAA16 transcription factor.…”

The Methylome of Soybean Roots during the Compatible Interaction with the Soybean Cyst Nematode

“…The soybean ubiquitin (Glyma.20G141600), a constitutively expressed gene, was used as an internal control to normalize gene expression levels. Quantification of gene expression changes in SCN-infected samples relative to noninfected control were performed as previously described by Hewezi et al (2015). The primer sequences used in qPCR analysis are provided in Supplemental Table S14.…”

Molecular Characterization of A Novel Effector Expansin-like Protein from Heterodera avenae that Induces Cell Death in Nicotiana benthamiana

“…Ultrastructural analysis of root cortical cells shows a small pore at the stylet orifice, supporting the idea effector proteins are delivered directly into the host cell cytoplasm51.A M. incognita effector protein, 7H08, containing nuclear localization signals (NLSs), was localized to the nuclei of plant cells, and showed transcriptional activation activity in both yeast and plant systems52. The 10A07 effector from H. schachtii is phosphorylated by a plant kinase in the cytoplasm and then translocated to the nucleus, interacting with the transcription factor IAA16 to promote parasitism53. Cell wall localization of HaEXPB2 provides direct evidence that nematode expansin proteins have an important function in the plant cell wall.…”