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Parasitism genes encoding secreted effector proteins of plant-parasitic nematodes play important roles in facilitating parasitism. An annexin-like gene was isolated from the cereal cyst nematode  Heterodera avenae  (termed  Ha-annexin ) and had high similarity to  annexin 2 , which encodes a secreted protein of  Globodera pallida .  Ha-annexin  encodes a predicted 326 amino acid protein containing four conserved annexin domains. Southern blotting revealed that there are at least two homologies in the  H .  avenae  genome.  Ha-annexin  transcripts were expressed within the subventral gland cells of the pre-parasitic second-stage juveniles by  in situ  hybridization. Additionally, expression of these transcripts were relatively higher in the parasitic second-stage juveniles by quantitative real-time RT-PCR analysis, coinciding with the time when feeding cell formation is initiated. Knockdown of  Ha-annexin  by method of barley stripe mosaic virus-based host-induced gene silencing (BSMV-HIGS) caused impaired nematode infections at 7 dpi and reduced females at 40 dpi, indicating important roles of the gene in parasitism at least in early stage  in vivo . Transiently expression of Ha-ANNEXIN in onion epidermal cells and  Nicotiana benthamiana  leaf cells showed the whole cell-localization. Using transient expression assays in  N .  benthamiana , we found that Ha-ANNEXIN could suppress programmed cell death triggered by the pro-apoptotic mouse protein BAX and the induction of marker genes of PAMP-triggered immunity (PTI) in  N .  benthamiana . In addition, Ha-ANNEXIN targeted a point in the mitogen-activated protein kinase (MAPK) signaling pathway downstream of two kinases MKK1 and NPK1 in  N .  benthamiana .

An ANNEXIN-Like Protein from the Cereal Cyst Nematode Heterodera avenae Suppresses Plant Defense