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Nontoxic Nep1-Like Proteins of the Downy Mildew Pathogen Hyaloperonospora arabidopsidis: Repression of Necrosis-Inducing Activity by a Surface-Exposed Region

May 2012 , Volume 25 , Number  5
Pages  697 - 708

Adriana Cabral,1 Stan Oome,1,2 Nick Sander,1 Isabell Küfner,3 Thorsten Nürnberger,3 and Guido Van den Ackerveken1,2

1Plant-microbe interactions, Department of Biology, Utrecht University, Padualaan 8, 3508 CH Utrecht, The Netherlands; 2Centre for BioSystems Genomics (CBSG), Wageningen University, Binnenhaven 5, 6709 PD Wageningen, The Netherlands; 3Zentrum für Molekularbiologie der Pflanzen-Pflanzenbiochemie, Eberhard-Karls-Universität Tübingen, Auf der Morgenstelle 5, D-72076 Tübingen, Germany

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Accepted 27 December 2011.

The genome of the downy mildew pathogen Hyaloperonospora arabidopsidis encodes necrosis and ethylene-inducing peptide 1 (Nep1)-like proteins (NLP). Although NLP are widely distributed in eukaryotic and prokaryotic plant pathogens, it was surprising to find these proteins in the obligate biotrophic oomycete H. arabidopsidis. Therefore, we analyzed the H. arabidopsidis NLP (HaNLP) family and identified 12 HaNLP genes and 15 pseudogenes. Most of the 27 genes form an H. arabidopsidis–specific cluster when compared with other oomycete NLP genes, suggesting this class of effectors has recently expanded in H. arabidopsidis. HaNLP transcripts were mainly detected during early infection stages. Agrobacterium tumefaciens–mediated transient expression and infiltration of recombinant NLP into tobacco and Arabidopsis leaves revealed that all HaNLP tested are noncytotoxic proteins. Even HaNLP3, which is most similar to necrosis-inducing NLP proteins of other oomycetes and which contains all amino acids that are critical for necrosis-inducing activity, did not induce necrosis. Chimeras constructed between HaNLP3 and the necrosis-inducing PsojNIP protein demonstrated that most of the HaNLP3 protein is functionally equivalent to PsojNIP, except for an exposed domain that prevents necrosis induction. The early expression and species-specific expansion of the HaNLP genes is suggestive of an alternative function of noncytolytic NLP proteins during biotrophic infection of plants.

© 2012 The American Phytopathological Society