Background <p>Cucumber (<i>Cucumis sativus</i> L.) is a globally important crop, yet its production is severely hampered by pathogen attacks, leading to substantial economic losses. Nucleotide-binding site-leucine-rich repeat (NLR) genes are critical components of the plant immune system, but a comprehensive understanding of their genetic diversity and evolutionary mechanisms in cucumber has been lacking.</p> Methods <p>Leveraging a cucumber pan-genome of 12 representative accessions, this study systematically investigated the NLR gene family through orthologous gene group (OGG) analysis, focusing on presence/absence variation (PAV), phylogeny, gene structure, integrated domains (IDs), NLR-pairs, copy number variation, and selection pressures. Publicly available transcriptome data were also integrated to analyze NLR gene expression patterns upon pathogen inoculation.</p> Results <p>This study identified a total of 879 pan-NLR genes, which were clustered into 33 core and 54 dispensable orthologous gene groups (OGGs). Comparative genomic analysis revealed that the cucumber NLR repertoire has undergone a contraction during its evolution. Phylogenetic analysis uncovered distinct evolutionary paths among NLR subfamilies: RNLs are highly conserved, CNLs and TNLs exhibit species-specific expansions, and NLs show a polyphyletic distribution, primarily arising from N-terminal domain loss events. Compared to wild populations (Indian), cultivated populations (especially the Eurasian group) exhibit reduced NLR diversity, mainly due to the loss of dispensable genes. This study identified specific IDs and NLR-pairs in wild germplasm, which are potentially associated with responses to specific pathogen pressures. Selection pressure analysis indicated that the NLR family is predominantly under purifying selection, although some genes experienced strong positive selection during domestication. Transcriptome analysis identified a candidate gene, <i>CsaV4_2G000768</i>, which contains a unique ID and shows a broad-spectrum response to multiple pathogens.</p> Conclusion <p>This study provides a systematic, pan-genomic view of the contraction and divergent evolution of the cucumber NLR gene family and elucidates the impact of domestication on its diversity. The identification of unique NLR-IDs and NLR-pairs from wild germplasm, along with a candidate gene potentially associated with broad-spectrum response, offers valuable theoretical insights and genetic resources for cucumber disease resistance breeding.</p>

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Pan-NLR gene family analyses decipher evolutionary dynamics, population diversity, and potential disease resistance genes in cucumber

  • Baohui Zhang,
  • Ying Deng

摘要

Background

Cucumber (Cucumis sativus L.) is a globally important crop, yet its production is severely hampered by pathogen attacks, leading to substantial economic losses. Nucleotide-binding site-leucine-rich repeat (NLR) genes are critical components of the plant immune system, but a comprehensive understanding of their genetic diversity and evolutionary mechanisms in cucumber has been lacking.

Methods

Leveraging a cucumber pan-genome of 12 representative accessions, this study systematically investigated the NLR gene family through orthologous gene group (OGG) analysis, focusing on presence/absence variation (PAV), phylogeny, gene structure, integrated domains (IDs), NLR-pairs, copy number variation, and selection pressures. Publicly available transcriptome data were also integrated to analyze NLR gene expression patterns upon pathogen inoculation.

Results

This study identified a total of 879 pan-NLR genes, which were clustered into 33 core and 54 dispensable orthologous gene groups (OGGs). Comparative genomic analysis revealed that the cucumber NLR repertoire has undergone a contraction during its evolution. Phylogenetic analysis uncovered distinct evolutionary paths among NLR subfamilies: RNLs are highly conserved, CNLs and TNLs exhibit species-specific expansions, and NLs show a polyphyletic distribution, primarily arising from N-terminal domain loss events. Compared to wild populations (Indian), cultivated populations (especially the Eurasian group) exhibit reduced NLR diversity, mainly due to the loss of dispensable genes. This study identified specific IDs and NLR-pairs in wild germplasm, which are potentially associated with responses to specific pathogen pressures. Selection pressure analysis indicated that the NLR family is predominantly under purifying selection, although some genes experienced strong positive selection during domestication. Transcriptome analysis identified a candidate gene, CsaV4_2G000768, which contains a unique ID and shows a broad-spectrum response to multiple pathogens.

Conclusion

This study provides a systematic, pan-genomic view of the contraction and divergent evolution of the cucumber NLR gene family and elucidates the impact of domestication on its diversity. The identification of unique NLR-IDs and NLR-pairs from wild germplasm, along with a candidate gene potentially associated with broad-spectrum response, offers valuable theoretical insights and genetic resources for cucumber disease resistance breeding.