Abstract
Cyst nematodes are sedentary plant parasites that cause dramatic cellular changes in the plant root to form feeding cells, so-called syncytia. 10A06 is a cyst nematode secretory protein that is most likely secreted as an effector into the developing syncytia during early plant parasitism. A homolog of the uncharacterized soybean cyst nematode (Heterodera glycines), 10A06 gene was cloned from the sugar beet cyst nematode (Heterodera schachtii), which is able to infect Arabidopsis (Arabidopsis thaliana). Constitutive expression of 10A06 in Arabidopsis affected plant morphology and increased susceptibility to H. schachtii as well as to other plant pathogens. Using yeast two-hybrid assays, we identified Spermidine Synthase2 (SPDS2), a key enzyme involved in polyamine biosynthesis, as a specific 10A06 interactor. In support of this protein-protein interaction, transgenic plants expressing 10A06 exhibited elevated SPDS2 mRNA abundance, significantly higher spermidine content, and increased polyamine oxidase (PAO) activity. Furthermore, the SPDS2 promoter was strongly activated in the nematode-induced syncytia, and transgenic plants overexpressing SPDS2 showed enhanced plant susceptibility to H. schachtii. In addition, in planta expression of 10A06 or SPDS2 increased mRNA abundance of a set of antioxidant genes upon nematode infection. These data lend strong support to a model in which the cyst nematode effector 10A06 exerts its function through the interaction with SPDS2, thereby increasing spermidine content and subsequently PAO activity. Increasing PAO activity results in stimulating the induction of the cellular antioxidant machinery in syncytia. Furthermore, we observed an apparent disruption of salicylic acid defense signaling as a function of 10A06. Most likely, increased antioxidant protection and interruption of salicylic acid signaling are key aspects of 10A06 function in addition to other physiological and morphological changes caused by altered polyamines, which are potent plant signaling molecules.
Highlights
Cyst nematodes are sedentary plant parasites that cause dramatic cellular changes in the plant root to form feeding cells, socalled syncytia. 10A06 is a cyst nematode secretory protein that is most likely secreted as an effector into the developing syncytia during early plant parasitism
Its host species, the 10A06 cDNA was identified from the sugar beet cyst nematode (H. schachtii), which can parasitize Arabidopsis
We have characterized the H. schachtii 10A06 effector protein, which is synthesized in the dorsal esophageal gland during early stages of parasitism, when the syncytium is developing. 10A06 belongs to a small gene family without similarity to proteins in databases, suggesting a unique functional role in cyst nematode parasitism
Summary
Cyst nematodes are sedentary plant parasites that cause dramatic cellular changes in the plant root to form feeding cells, socalled syncytia. 10A06 is a cyst nematode secretory protein that is most likely secreted as an effector into the developing syncytia during early plant parasitism. Feeding site initiation and formation are characterized by complex morphological and physiological changes of the parasitized plant root cells This process includes endoreduplication, cell wall modification and dissolution leading to cell fusion, disappearance of large vacuoles, increased numbers of organelles, and metabolic activity. A growing body of evidence shows that secreted proteins encoded by nematode parasitism genes act as effector molecules and play the central role in the initiation and formation of the feeding sites (Wang et al, 2005; Huang et al, 2006a, 2006b; Hewezi et al, 2008). Expression in the host plants of several effector genes identified by this approach affected plant phenotypes and nematode susceptibility (Doyle and Lambert, 2003; Wang et al, 2005; Huang et al, 2006b; Hewezi et al, 2008), validating esophageal gland effector protein involvement in plant parasitism
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