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ARS Home » Northeast Area » Ithaca, New York » Robert W. Holley Center for Agriculture & Health » Emerging Pests and Pathogens Research » Research » Publications at this Location » Publication #283670
Title: A ubiquitin carboxyl extension protein secreted from a plant-parasitic nematode Globodera rostochiensis is cleaved in planta to promote plant parasitism

Author
item Chronis, Demosthenis
item CHEN, SHIYAN - Cornell University
item Lu, Shunwen
item HEWEZI, TAREK - Iowa State University
item CARPENTER, SARA - Cornell University
item BAUM, THOMAS - Iowa State University
item LORIA, ROSEMARY - Cornell University
item Wang, Xiaohong

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/17/2013
Publication Date: 4/15/2013
Citation: Chronis, D.N., Chen, S., Lu, S., Hewezi, T., Carpenter, S.C., Baum, T.J., Loria, R., Wang, X. 2013. A ubiquitin carboxyl extension protein secreted from a plant-parasitic nematode Globodera rostochiensis is cleaved in planta to promote plant parasitism. Plant Journal. 74(2):185-196.

Interpretive Summary: The golden potato cyst nematode (a.k.a. golden nematode or GN) is a devastating and quarantine pest that threatens the US potato industry. This potato pest secrets effector proteins through their stylet (a mouth spear) into plant root cells to manipulate host cellular processes for successful infection. We have cloned and functionally characterized an effector gene (GrUbi) encoding a unique ubiquitin extension protein (UBI) from GN. Using in planta overexpression and host-derived RNAi approaches, we provided direct evidence that this nematode secreted UBI plays an important role in nematode parasitism. Interestingly, we found that this nematode UBI could be processed in planta to release free ubiquitin and a short peptide (GrCEP12). Results from analyzing transgenic potato lines overexpressing the GrUbi gene suggested that the derived free ubiquitin might interfere with the function of the 26S proteasome, an essential component of the ubiquitin/proteasome system, to suppress plant defense. In addition, we provided evidence that the derived GrCEP12 peptide could also suppress plant defense. This study provides new evidence that nematodes use secreted effectors to suppress plant immunity to enable their successful infection. Knowledge developed from this study might be useful for generating engineered nematode resistance in potato.

Technical Abstract: Nematode effectors originated from the esophageal gland secretory cells play a role in suppressing plant defense thereby allowing the formation of feeding cells that necessitates the growth and development of cyst nematode species. A gene (GrUbi) encoding a unique ubiquitin extension protein (UBI) that consists of a signal peptide for secretion, a monoubiquitin domain, and a carboxyl extension protein (CEP) domain was cloned from the potato cyst nematode Globodera rostochiensis. This GrUbi gene was expressed exclusively within the nematode’s dorsal gland cell and highly upregulated in the parasitic second-stage juvenile correlating to the time when feeding cells start to be initiated. We found that specific knocking-down of GrUbi transcripts through host-derived RNA interference reduced nematode parasitic success and that constitutive expression of GrUbi in potato resulted in increased nematode susceptibility, providing direct evidence that GrUBI is involved in plant parasitism. Using transient expression assays in Nicotiana benthamiana leaves, we found that GrUBI was processed into free ubiquitin and a 12-aa CEP in planta and that the derived CEP could suppress cell death triggered by two resistance genes. A target search showed that the expression of a subunit of the 26S proteasome that has been implicated in defense was dramatically suppressed in G. rostochiensis-infected potato roots and in GrUbi overexpressing potato lines. Together, these results suggest that both derived proteins of GrUBI act to suppress plant defense potentially through modulating the function of the 26S proteasome and other pathway(s) to promote feeding cell formation.