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Background  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.    Results  Here 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.    Conclusions  Our 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.    Supplementary information   Supplementary information  accompanies this paper at 10.1186/s12864-020-07146-0.

A new esophageal gland transcriptome reveals signatures of large scale de novo effector birth in the root lesion nematode Pratylenchus penetrans