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JXB Advance Access published online on November 3, 2009
Journal of Experimental Botany, doi:10.1093/jxb/erp293
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© 2009 The Author(s).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)

RESEARCH PAPER

A nematode effector protein similar to annexins in host plants

Nrupali Patel1 *, Noureddine Hamamouch1, Chunying Li1, Tarek Hewezi2, Richard S. Hussey3, Thomas J. Baum2, Melissa G. Mitchum4 and Eric L. Davis1,{dagger}

1Department of Plant Pathology, North Carolina State University, Raleigh, NC 27607, USA
2Department of Plant Pathology, Iowa State University, Ames, IA 50011, USA
3Department of Plant Pathology, University of Georgia, Athens, GA 30602, USA
4Division of Plant Sciences and Bond Life Sciences Center, University of Missouri, Columbia 65211, USA

{dagger} To whom correspondence should be addressed: E-mail: eric_davis{at}ncsu.edu

Nematode parasitism genes encode secreted effector proteins that play a role in host infection. A homologue of the expressed Hg4F01 gene of the root-parasitic soybean cyst nematode, Heterodera glycines, encoding an annexin-like effector, was isolated in the related Heterodera schachtii to facilitate use of Arabidopsis thaliana as a model host. Hs4F01 and its protein product were exclusively expressed within the dorsal oesophageal gland secretory cell in the parasitic stages of H. schachtii. Hs4F01 had a 41% predicted amino acid sequence identity to the nex-1 annexin of C. elegans and 33% identity to annexin-1 (annAt1) of Arabidopsis, it contained four conserved domains typical of the annexin family of calcium and phospholipid binding proteins, and it had a predicted signal peptide for secretion that was present in nematode annexins of only Heterodera spp. Constitutive expression of Hs4F01 in wild-type Arabidopsis promoted hyper-susceptibility to H. schachtii infection. Complementation of an AnnAt1 mutant by constitutive expression of Hs4F01 reverted mutant sensitivity to 75mM NaCl, suggesting a similar function of the Hs4F01 annexin-like effector in the stress response by plant cells. Yeast two-hybrid assays confirmed a specific interaction between Hs4F01 and an Arabidopsis oxidoreductase member of the 2OG-Fe(II) oxygenase family, a type of plant enzyme demonstrated to promote susceptibility to oomycete pathogens. RNA interference assays that expressed double-stranded RNA complementary to Hs4F01 in transgenic Arabidopsis specifically decreased parasitic nematode Hs4F01 transcript levels and significantly reduced nematode infection levels. The combined data suggest that nematode secretion of an Hs4F01 annexin-like effector into host root cells may mimic plant annexin function during the parasitic interaction.

Key words: Arabidopsis thaliana, cyst nematode, Heterodera, parasitism gene, RNAi, secretions

* Present address: Department of Plant Biology and Pathology, Rutgers University, New Brunswick, NJ 08901, USA.

Received 11 August 2009; Revised 8 September 2009 Accepted 9 September 2009


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