Abstract

BackgroundThe root lesion nematode Pratylenchus penetrans is a migratory plant-parasitic nematode responsible for economically important losses in a wide number of crops. Despite the importance of P. penetrans, the molecular mechanisms employed by this nematode to promote virulence remain largely unknown.ResultsHere we generated a new and comprehensive esophageal glands-specific transcriptome library for P. penetrans. In-depth analysis of this transcriptome enabled a robust identification of a catalogue of 30 new candidate effector genes, which were experimentally validated in the esophageal glands by in situ hybridization. We further validated the expression of a multifaceted network of candidate effectors during the interaction with different plants. To advance our understanding of the “effectorome” of P. penetrans, we adopted a phylogenetic approach and compared the expanded effector repertoire of P. penetrans to the genome/transcriptome of other nematode species with similar or contrasting parasitism strategies. Our data allowed us to infer plausible evolutionary histories that shaped the effector repertoire of P. penetrans, as well as other close and distant plant-parasitic nematodes. Two remarkable trends were apparent: 1) large scale effector birth in the Pratylenchidae in general and P. penetrans in particular, and 2) large scale effector death in sedentary (endo) plant-parasitic nematodes.ConclusionsOur study doubles the number of validated Pratylenchus penetrans effectors reported in the literature. The dramatic effector gene gain in P. penetrans could be related to the remarkable ability of this nematode to parasitize a large number of plants. Our data provide valuable insights into nematode parasitism and contribute towards basic understating of the adaptation of P. penetrans and other root lesion nematodes to specific host plants.

Highlights

  • The root lesion nematode Pratylenchus penetrans is a migratory plant-parasitic nematode responsible for economically important losses in a wide number of crops

  • A more complete roster of candidate effector genes of Pratylenchus penetrans The current library generated from the esophageal glands of P. penetrans resulted in ~ 150 million raw reads

  • The raw reads were cleaned and approximately 99 million high-quality reads were mapped against the 23, 715 transcripts previously generated from the same P. penetrans isolate [13], and against the genomic sequence of the recently discovered root lesion nematode virus 1, which was found to be associated with the same nematode isolate [16]

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Summary

Introduction

The root lesion nematode Pratylenchus penetrans is a migratory plant-parasitic nematode responsible for economically important losses in a wide number of crops. Despite the importance of P. penetrans, the molecular mechanisms employed by this nematode to promote virulence remain largely unknown. Members of the Pratylenchus genus are known as root lesion nematodes (RLNs) and belong to the third most important group of plant-parasitic nematodes (PPNs) [3]. One of the common features of these migratory nematodes is their dynamic behavior within the host roots, i.e. nematodes do not become sedentary and are able to migrate in and out of the roots, causing extensive damage as they do so. Once inside of the roots, nematodes migrate and feed almost exclusively from the cortical cells, where they cause mechanical damage, browning, and necrosis of the root tissue. The molecular mechanisms that RLNs employ to promote virulence remain largely unknown

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