The novel cyst nematode effector protein 30D08 targets host nuclear functions to alter gene expression in feeding sites

New Phytol. 2018 Jul;219(2):697-713. doi: 10.1111/nph.15179. Epub 2018 May 4.

Abstract

Cyst nematodes deliver effector proteins into host cells to manipulate cellular processes and establish a metabolically hyperactive feeding site. The novel 30D08 effector protein is produced in the dorsal gland of parasitic juveniles, but its function has remained unknown. We demonstrate that expression of 30D08 contributes to nematode parasitism, the protein is packaged into secretory granules and it is targeted to the plant nucleus where it interacts with SMU2 (homolog of suppressor of mec-8 and unc-52 2), an auxiliary spliceosomal protein. We show that SMU2 is expressed in feeding sites and an smu2 mutant is less susceptible to nematode infection. In Arabidopsis expressing 30D08 under the SMU2 promoter, several genes were found to be alternatively spliced and the most abundant functional classes represented among differentially expressed genes were involved in RNA processing, transcription and binding, as well as in development, and hormone and secondary metabolism, representing key cellular processes known to be important for feeding site formation. In conclusion, we demonstrated that the 30D08 effector is secreted from the nematode and targeted to the plant nucleus where its interaction with a host auxiliary spliceosomal protein may alter the pre-mRNA splicing and expression of a subset of genes important for feeding site formation.

Keywords: Heterodera; SMU2; alternative splicing; cyst nematode; effector; nucleus; spliceosome; syncytium.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Alternative Splicing / genetics
  • Amino Acid Sequence
  • Animals
  • Arabidopsis / genetics*
  • Arabidopsis / parasitology*
  • Cell Nucleus / metabolism*
  • Feeding Behavior*
  • Gene Expression Regulation, Plant*
  • Genes, Plant
  • Helminth Proteins / chemistry
  • Helminth Proteins / metabolism*
  • Host-Parasite Interactions / genetics*
  • Life Cycle Stages
  • Nuclear Localization Signals
  • Parasites / metabolism
  • Plant Cells / metabolism
  • Plant Leaves / metabolism
  • Plant Roots / growth & development
  • Plant Roots / metabolism
  • Plant Roots / parasitology
  • Promoter Regions, Genetic / genetics
  • Protein Binding
  • RNA Interference
  • Seedlings / metabolism
  • Tylenchoidea / growth & development
  • Tylenchoidea / metabolism*
  • Up-Regulation

Substances

  • Helminth Proteins
  • Nuclear Localization Signals

Associated data

  • GENBANK/MF959551