The GpIA7 effector from the potato cyst nematode Globodera pallida targets potato EBP1 and interferes with the plant cell cycle programme.

Mirela C Coke,Adams Chande,Daniel S Shaw,Sophie Mantelin,John T Jones,Peter Thorpe,Catherine J Lilley,Peter E Urwin,Kathryn M Wright

doi:10.1093/jxb/erab353

Abstract

The potato cyst nematode Globodera pallida acquires all of its nutrients from an elaborate feeding site that it establishes in a host plant root. Normal development of the root cells is re-programmed in a process coordinated by secreted nematode effector proteins. The biological function of the G. pallida GpIA7 effector was investigated in this study. GpIA7 is specifically expressed in the subventral pharyngeal glands of pre-parasitic stage nematodes. Ectopic expression of GpIA7 in potato plants affected plant growth and development, suggesting a potential role for this effector in feeding site establishment. Potato plants overexpressing GpIA7 were shorter, with reduced tuber weight and delayed flowering. We provide evidence that GpIA7 associates with the plant growth regulator StEBP1 (ErbB-3 epidermal growth factor receptor-binding protein 1). GpIA7 modulates the regulatory function of StEBP1, altering the expression level of downstream target genes, including ribonucleotide reductase 2, cyclin D3;1, and retinoblastoma related 1, which are down-regulated in plants overexpressing GpIA7. We provide an insight into the molecular mechanism used by the nematode to manipulate the host cell cycle and demonstrate that this may rely, at least in part, on hindering the function of host EBP1.

Highlights

The potato cyst nematode Globodera pallida is a sedentary endo- from eggs enclosed in cysts in response to host root exudates. parasitic nematode that has a close biotrophic relationship Following chemical cues, the J2s locate a host root, penetrate with its host
The GPLIN_000740500 paralogue displays a similar pattern, some expression is maintained until 7 dpi, suggesting that GpIA7 transcript might peak around the moment of infection or syncytium induction, decrease over several days.This temporal expression profile was confirmed by quantitative reverse transcription–PCR (qRT–PCR) analysis, which shows that the expression of the GpIA7 paralogues is highly induced in J2s and remains high in parasitic nematodes established in roots at 5 dpi (Supplementary Fig. S1G)
GpIA7 proved to be refractory to reduction of StEBP1 transcripts in the EBP1 (RNAi) by soaking J2 nematodes in dsRNA that targeted transcripts from both paralogues; no reduction in transcript abundance was detected by qRT–PCR on multiple experimental occasions (Supplementary Fig. S3)

Summary

Introduction

The potato cyst nematode Globodera pallida is a sedentary endo- from eggs enclosed in cysts in response to host root exudates. parasitic nematode that has a close biotrophic relationship Following chemical cues, the J2s locate a host root, penetrate with its host. Syncytial nuclei become enlarged and lobed soon after feeding site induction, and it has been suggested that they undergo endoreduplication (Golinowski et al, 1996) These elaborate changes in plant cells that culminate in the formation of the syncytial feeding site are thought to be orchestrated by effector proteins from the nematode secretions, which are mainly produced in the pharyngeal glands of the nematode and injected into the selected host cell through the stylet. Bellafiore et al, 2008; Maier et al, 2013; Thorpe et al, 2014) revealed that the majority of effectors are pioneers with no sequence similarity to known proteins Their functions in the plant cell cannot be predicted and our knowledge of the molecular mechanisms used by the nematode to re-route the cells’ normal growth and development processes is fragmented

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Conclusion