Skip to main content
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 #300807

Title: Phenotypic analysis of apoplastic effectors from the phytopathogenic nematode, Globodera rostochiensis demonstrates that an expansin can induce and suppress host defenses

item ALI, SHAWKAT - Universite De Sherbrooke
item MAGNE, MAXIM - Universite De Sherbrooke
item CHEN, SHIYAN - Cornell University
item COTE, OLIVIER - Universite De Sherbrooke
item STARE, BARBARA GERIC - Agricultural Institute Of Slovenia
item OBRADOVIC, NATASA - Universite De Sherbrooke
item JAMSHAID, LUBNA - Universite De Sherbrooke
item Wang, Xiaohong
item BELAIR, GUY - Agriculture And Agri-Food Canada
item MOFFETT, PETER - Universite De Sherbrooke

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/18/2014
Publication Date: 1/21/2015
Citation: Ali, S., Magne, M., Chen, S., Cote, O., Stare, B., Obradovic, N., Jamshaid, L., Wang, X., Belair, G., Moffett, P. 2015. Phenotypic analysis of apoplastic effectors from the phytopathogenic nematode, Globodera rostochiensis demonstrates that an expansin can induce and suppress host defenses. PLoS One. DOI: 10.1371/journal.pone.0115042.

Interpretive Summary: The golden potato cyst nematode (a.k.a. golden nematode) is a quarantine pest of potato that threatens the potato industry worldwide. Like other plant pathogens, this potato pest secretes multiple effector proteins into root cells to enable successful infection. In this study, we used computational approaches and identified more than 30 effector protein genes from the golden nematode. We further developed in planta expression assays to investigate the potential function of these effector proteins in parasitism. Our results suggested that these effectors are involved in host defense suppression, manipulation of host cell development and metabolism, as well as modification of host cell walls to facilitate nematode infection. This study is significant because discovering and understanding the function of nematode-secreted effectors is necessary for uncovering the molecular mechanisms of golden nematode infection on potato.

Technical Abstract: The potato cyst nematode Globodera rostochiensis (Woll.) is an important pest of potato. Like other biotrophic pathogens, plant parasitic nematodes are presumed to employ effector proteins, secreted into the apoplast as well as the host cytoplasm to successfully infect their hosts. We have identified at least fifteen G. rostochiensis genes encoding predicted apoplastic effector proteins from public databases. To gain insight into how such proteins affect host biology, we have generated a library of ORFs encoding predicted G. rostochiensis apoplastic effectors in vectors for in planta expression and expressed these in Nicotiana benthamiana, N. tabacum, tomato and potato. Approximately half of the putative effectors produced dramatic phenotypes when expressed systemically in N. benthamiana from Potato virus X (PVX) based constructs. Consistent with previous reports, several CLAVATA3/ESR-like proteins induced marked developmental phenotypes, suggesting that nematodes have the capacity to reprogram cell identity. Several predicted cell wall-modifying proteins induced necrosis and chlorosis, consistent with roles in tissue invasion. In addition, we identified two effectors that were able to suppress defense responses. These defense suppressors included an ubiquitin extension protein (GrUBCEP12) as well as an expansin-like protein (GrEXPB2). Surprisingly, these apoplastic effectors suppressed cell death induced by elicitors as well R gene signaling induced in the cytoplasm suggesting that intra-cellular defense responses can be modulated by extracellular factors. At the same time, GrEXPB2 elicited defense response in species- and sequence- specific manners, suggesting that this effector can also be recognized by the plant immune system. Our characterization of G. rostochiensis apoplastic effector proteins suggest that, like other pathogens, potato cyst nematodes secrete effectors that can induce or suppress host defenses, but in addition, encode subsets of effectors that modulate host cell development and metabolism as well as modifying host cell walls.