The potato RNA metabolism machinery is targeted by the cyst nematode effector RHA1B for successful parasitism

The potato (Solanum tuberosum) cyst nematode Globodera pallida induces a multinucleate feeding site (syncytium) in potato roots as its sole source of nutrition. Here, we demonstrate that the G. pallida effector RING-H2 finger A1b (RHA1B), which is a functional ubiquitin ligase, interferes with the carbon catabolite repression 4 (CCR4)-negative on TATA-less (NOT) deadenylase-based RNA metabolism machinery that regulates syncytium development in G. pallida-infected potato. Specifically, RHA1B targets the CCR4-associated factor 1 (CAF1) and StNOT10 subunits of the CCR4-NOT complex for proteasome-mediated degradation, leading to upregulation of the cyclin gene StCycA2 involved in syncytium formation. The StCAF1 subunit of CCR4-NOT recruits the RNA binding protein StPUM5 to deadenylate StCycA2 mRNA, resulting in shortened poly-A tails of StCycA2 mRNA and subsequently reduced transcript levels. Knockdown of either subunit (StCAF1 or StNOT10) of the CCR4-NOT complex or StPUM5 in transgenic potato plants resulted in enlarged syncytia and enhanced susceptibility to G. pallida infection, which resembles the phenotypes of StCycA2 overexpression transgenic potato plants. Genetic analyses indicate that transgenic potato plants overexpressing RHA1B exhibit similar phenotypes as transgenic potato plants with knockdown of StNOT10, StCAF1, or StPUM5. Thus, our data suggest that G. pallida utilizes the RHA1B effector to manipulate RNA metabolism in host plants, thereby promoting syncytium development for parasitic success.