Abstract
The burrowing nematode, Radopholus similis, is an economically important plant-parasitic nematode that inflicts damage and yield loss to a wide range of crops. This migratory endoparasite is widely distributed in warmer regions and causes extensive destruction to the root systems of important food crops (e.g., citrus, banana). Despite the economic importance of this nematode, little is known about the repertoire of effectors owned by this species. Here we combined spatially and temporally resolved next-generation sequencing datasets of R. similis to select a list of candidates for the identification of effector genes for this species. We confirmed spatial expression of transcripts of 30 new candidate effectors within the esophageal glands of R. similis by in situ hybridization, revealing a large number of pioneer genes specific to this nematode. We identify a gland promoter motif specifically associated with the subventral glands (named Rs-SUG box), a putative hallmark of spatial and concerted regulation of these effectors. Nematode transcriptome analyses confirmed the expression of these effectors during the interaction with the host, with a large number of pioneer genes being especially abundant. Our data revealed that R. similis holds a diverse and emergent repertoire of effectors, which has been shaped by various evolutionary events, including neofunctionalization, horizontal gene transfer, and possibly by de novo gene birth. In addition, we also report the first GH62 gene so far discovered for any metazoan and putatively acquired by lateral gene transfer from a bacterial donor. Considering the economic damage caused by R. similis, this information provides valuable data to elucidate the mode of parasitism of this nematode.
Highlights
The burrowing nematode Radopholus similis is an important plant-pathogen that inflicts damage and yield losses to a broad range of crops
We identified new exclusive examples of horizontal gene transfer (HGT) events to this species, including the first gene belonging to the glycosyl hydrolase 62 (GH62) family ever described for a metazoan
To identify the R. similis homologues of previously described effectors in plant-parasitic nematodes, a targeted effector search was performed based on sequence similarity [either using BLAST or the presence of characteristic protein domains of previously described carbohydrate-active enzymes (CAZymes)]
Summary
The burrowing nematode Radopholus similis is an important plant-pathogen that inflicts damage and yield losses to a broad range of crops This species is considered to be among the top 10 most damaging plant-parasitic nematodes world-wide [1]. Radopholus similis is widely distributed in warm subtropical and tropical regions, including South America, the Caribbean, Africa, Asia, and the Pacific Islands [2,3]. This nematode has been recurrently found in temperate regions (e.g., Europe) as a consequence of transporting infested plant material, causing noteworthy problems on ornamental glasshouse crops [4]. Radopholus similis is of great economic importance in commercial banana plantations as the causative agent of “toppling” disease impacting an important food resource of the people living in these areas [5,6]
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