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Main conclusion  Genome - wide annotation reveals that the gene birth–death process of the  Cucurbita  R family is associated with a species-specific diversification of TNL and CNL protein classes.    Abstract  The Cucurbitaceae family includes nearly 1000 plant species known universally as cucurbits.  Cucurbita  genus includes many economically important worldwide crops vulnerable to more than 200 pathogens. Therefore, the identification of pathogen-recognition genes is of utmost importance for this genus. The major class of plant-resistance (R) genes encodes nucleotide-binding site and leucine-rich repeat (NLR) proteins, and is divided into three sub-classes namely, TIR-NB-LRR (TNL), CC-NB-LRR (CNL) and RPW8-NB-LRR (RNL). Although the characterization of the NLR gene family has been carried out in important  Cucurbita  species, this information is still linked to the availability of sequenced genomes. In this study, we analyzed 40 de novo transcriptomes and 5 genome assemblies, which were explored to investigate the  Cucurbita  expressed-NLR (eNLR) and NLR repertoires using an ad hoc gene annotation approach. Over 1850 NLR-encoding genes were identified, finely characterized and compared to 96 well-characterized plant R-genes. The maximum likelihood analyses revealed an unusual diversification of CNL/TNL genes and a strong RNL conservation. Indeed, several gene gain and loss events have shaped the  Cucurbita  NLR family. Finally, to provide a first validation step  Cucurbita , eNLRs were explored by real-time PCR analysis. The NLR repertories of the 12  Cucurbita  species presented in this paper will be useful to discover novel R-genes.    Supplementary Information  The online version contains supplementary material available at 10.1007/s00425-021-03717-x.

Large-scale gene gains and losses molded the NLR defense arsenal during the Cucurbita evolution