{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T16:17:38Z","timestamp":1785428258110,"version":"3.56.0"},"reference-count":44,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2026,7,24]],"date-time":"2026-07-24T00:00:00Z","timestamp":1784851200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["32341044"],"award-info":[{"award-number":["32341044"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["32472751"],"award-info":[{"award-number":["32472751"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"award":["32341044"],"award-info":[{"award-number":["32341044"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"award":["32472751"],"award-info":[{"award-number":["32472751"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"name":"China Agriculture Research System of MOF and MARA","award":["CARS-23-G44"],"award-info":[{"award-number":["CARS-23-G44"]}]},{"award":["CARS-23-G44"],"award-info":[{"award-number":["CARS-23-G44"]}],"id":[{"id":"https:\/\/ror.org\/03p5eky76","id-type":"ROR","asserted-by":"publisher"}]},{"name":"Zhejiang Provincial Major Agricultural Technology Collaborative Promotion Plan Project","award":["2025ZDXT07-03"],"award-info":[{"award-number":["2025ZDXT07-03"]}]},{"name":"Zhejiang Provincial Key Research and Development Program Project","award":["2026C02A1024"],"award-info":[{"award-number":["2026C02A1024"]}]},{"name":"Local Cooperation Projects of Zhejiang Academy of Agricultural Sciences","award":["2026R23A77S001"],"award-info":[{"award-number":["2026R23A77S001"]}]},{"award":["2026R23A77S001"],"award-info":[{"award-number":["2026R23A77S001"]}],"id":[{"id":"https:\/\/ror.org\/02qbc3192","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Background\/Objectives: Nucleotide-binding leucine-rich repeat (NLR) proteins are major intracellular immune receptors involved in effector-triggered immunity. However, the evolutionary diversity and genomic organization of NLR repertoires remain incompletely characterized in Solanaceae crops and their wild relatives. This study aimed to investigate the pan-NLRome landscape and evolutionary patterns of tomato and related species. Methods: A comparative pan-NLRome analysis was performed across five angiosperms, including cultivated tomato (Solanum lycopersicum) and four related species (Solanum chilense, Solanum lycopersicoides, Solanum pimpinellifolium, and Arabidopsis thaliana). NLR genes were identified using an integrated HMMER- and BLASTp-based pipeline, followed by chromosome anchoring, orthogroup (OG) classification, phylogenetic analysis, spatial organization analysis, and evaluation of associations with long terminal repeat (LTR) retrotransposons. Results: A total of 1566 chromosome-anchored NLR genes were assigned to 150 OGs. Core OGs represented 25.3% of total OG diversity but contained a large proportion of NLR genes. Rarefaction analysis indicated continuous accumulation of novel OGs with increasing species sampling, supporting an open pan-NLRome structure. Phylogenetic analysis identified 18 NLR subfamilies, with SF_03 and SF_01 together accounting for approximately 79% of NLR genes. Dispersed homologs represented the predominant spatial arrangement pattern, accounting for 85.1% of NLR gene pairs across Solanaceae species. Conclusions: This study provides a comparative genomic framework for understanding NLR diversity and evolution in tomato and related Solanum species, highlighting the dynamic expansion and spatial organization of plant immune receptor repertoires and providing valuable resources for resistance gene discovery.<\/jats:p>","DOI":"10.3390\/genes17080864","type":"journal-article","created":{"date-parts":[[2026,7,27]],"date-time":"2026-07-27T16:11:56Z","timestamp":1785168716000},"page":"864","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Pan-NLRome Analysis of Cultivated Tomato and Wild Solanum Relatives Reveals an Open Immune Repertoire Dominated by Spatially Dispersed Homologs"],"prefix":"10.3390","volume":"17","author":[{"given":"Shibo","family":"Meng","sequence":"first","affiliation":[{"name":"College of Horticulture, Anhui Agricultural University, Hefei 230036, China"},{"name":"State Key Laboratory for Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiajun","family":"Zhu","sequence":"additional","affiliation":[{"name":"College of Horticulture, Anhui Agricultural University, Hefei 230036, China"},{"name":"State Key Laboratory for Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Enmei","family":"Hu","sequence":"additional","affiliation":[{"name":"Department of Agronomy and Horticulture, Jiangsu Vocational College of Agriculture and Forestry, Jurong 212400, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jia","family":"Liu","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4740-1843","authenticated-orcid":false,"given":"Yuan","family":"Cheng","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meiying","family":"Ruan","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chenxu","family":"Liu","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qingjing","family":"Ye","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rongqing","family":"Wang","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhuping","family":"Yao","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-8068-8574","authenticated-orcid":false,"given":"Zhimiao","family":"Li","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guozhi","family":"Zhou","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7426-498X","authenticated-orcid":false,"given":"Hongjian","family":"Wan","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural 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Cell"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1105\/tpc.17.00579","article-title":"Defended to the Nines: 25 Years of Resistance Gene Cloning Identifies Nine Mechanisms for R Protein Function","volume":"30","author":"Kourelis","year":"2018","journal-title":"Plant Cell"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1260","DOI":"10.1016\/j.cell.2019.07.038","article-title":"A Species-Wide Inventory of NLR Genes and Alleles in Arabidopsis thaliana","volume":"178","author":"Monteiro","year":"2019","journal-title":"Cell"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"eaav5870","DOI":"10.1126\/science.aav5870","article-title":"Reconstitution and structure of a plant NLR resistosome conferring immunity","volume":"364","author":"Wang","year":"2019","journal-title":"Science"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3528","DOI":"10.1016\/j.cell.2021.05.003","article-title":"The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling","volume":"184","author":"Bi","year":"2021","journal-title":"Cell"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"eabq3297","DOI":"10.1126\/science.abq3297","article-title":"Identification and receptor mechanism of TIR-catalyzed small molecules in plant immunity","volume":"377","author":"Huang","year":"2022","journal-title":"Science"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2370","DOI":"10.1016\/j.cell.2022.04.032","article-title":"TIR domains of plant immune receptors are 2\u2032,3\u2032-cAMP\/cGMP synthetases mediating cell death","volume":"185","author":"Yu","year":"2022","journal-title":"Cell"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.coi.2019.12.007","article-title":"Plant NLR-triggered immunity: From receptor activation to downstream signaling","volume":"62","author":"Lolle","year":"2020","journal-title":"Curr. Opin. Immunol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.cell.2020.05.021","article-title":"Major Impacts of Widespread Structural Variation on Gene Expression and Crop Improvement in Tomato","volume":"182","author":"Alonge","year":"2020","journal-title":"Cell"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1186\/s13059-020-02224-8","article-title":"How the pan-genome is changing crop genomics and improvement","volume":"22","author":"Qiu","year":"2021","journal-title":"Genome Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"914","DOI":"10.1038\/s41477-020-0733-0","article-title":"Plant pan-genomes are the new reference","volume":"6","author":"Bayer","year":"2020","journal-title":"Nat. Plants"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1044","DOI":"10.1038\/s41588-019-0410-2","article-title":"The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor","volume":"51","author":"Gao","year":"2019","journal-title":"Nat. Genet."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1038\/s41586-022-04808-9","article-title":"Graph pangenome captures missing heritability and empowers tomato breeding","volume":"606","author":"Zhou","year":"2022","journal-title":"Nature"},{"key":"ref_15","first-page":"1205","article-title":"Genome-Wide Comparative Analyses Reveal the Dynamic Evolution of Nucleotide-Binding Leucine-Rich Repeat Gene Family among Solanaceae Plants","volume":"7","author":"Seo","year":"2016","journal-title":"DNA Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"D412","DOI":"10.1093\/nar\/gkaa913","article-title":"Pfam: The protein families database in 2021","volume":"49","author":"Mistry","year":"2020","journal-title":"Nucleic Acids Res."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Eddy, S.R. (2011). Accelerated Profile HMM Searches. PLoS Comput. Biol., 7.","DOI":"10.1371\/journal.pcbi.1002195"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1186\/s13059-019-1832-y","article-title":"OrthoFinder: Phylogenetic orthology inference for comparative genomics","volume":"20","author":"Emms","year":"2019","journal-title":"Genome Biol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"The Tomato Genome Consortium (2012). The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 485, 635.","DOI":"10.1038\/nature11119"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"iyae027","DOI":"10.1093\/genetics\/iyae027","article-title":"The Arabidopsis Information Resource in 2024","volume":"227","author":"Reiser","year":"2024","journal-title":"Genetics"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1093\/nar\/25.17.3389","article-title":"Gapped BLAST and PSI-BLAST: A new generation of protein database search programs","volume":"25","author":"Altschul","year":"1997","journal-title":"Nucleic Acids Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1639","DOI":"10.1101\/gr.092759.109","article-title":"Circos: An information aesthetic for comparative genomics","volume":"19","author":"Krzywinski","year":"2009","journal-title":"Genome Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e49","DOI":"10.1093\/nar\/gkr1293","article-title":"MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity","volume":"40","author":"Wang","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2498","DOI":"10.1101\/gr.1239303","article-title":"Cytoscape: A software environment for integrated models of biomolecular interaction networks","volume":"13","author":"Shannon","year":"2003","journal-title":"Genome Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1093\/molbev\/mst010","article-title":"MAFFT multiple sequence alignment software version 7: Improvements in performance and usability","volume":"30","author":"Katoh","year":"2013","journal-title":"Mol. Biol. Evol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1972","DOI":"10.1093\/bioinformatics\/btp348","article-title":"trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses","volume":"25","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Price, M.N., Dehal, P.S., and Arkin, A.P. (2010). FastTree 2\u2014Approximately maximum-likelihood trees for large alignments. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0009490"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"W293","DOI":"10.1093\/nar\/gkab301","article-title":"Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation","volume":"49","author":"Letunic","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"W265","DOI":"10.1093\/nar\/gkm286","article-title":"LTR_FINDER: An efficient tool for the prediction of full-length LTR retrotransposons","volume":"35","author":"Xu","year":"2007","journal-title":"Nucleic Acids Res."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Ellinghaus, D., Kurtz, S., and Willhoeft, U. (2008). LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinform., 9.","DOI":"10.1186\/1471-2105-9-18"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1410","DOI":"10.1104\/pp.17.01310","article-title":"LTR_retriever: A Highly Accurate and Sensitive Program for Identification of Long Terminal Repeat Retrotransposons","volume":"176","author":"Ou","year":"2017","journal-title":"Plant Physiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing","volume":"57","author":"Benjamini","year":"1995","journal-title":"J. R. Stat. Soc. Ser. B (Methodol.)"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"998","DOI":"10.1093\/plcell\/koab013","article-title":"Analysis of intraspecies diversity reveals a subset of highly variable plant immune receptors and predicts their binding sites","volume":"33","author":"Prigozhin","year":"2021","journal-title":"Plant Cell"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1038\/s41586-020-2947-8","article-title":"The barley pan-genome reveals the hidden legacy of mutation breeding","volume":"588","author":"Jayakodi","year":"2020","journal-title":"Nature"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1104\/pp.19.01273","article-title":"The NLR-Annotator Tool Enables Annotation of the Intracellular Immune Receptor Repertoire","volume":"183","author":"Steuernagel","year":"2020","journal-title":"Plant Physiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"e70257","DOI":"10.1002\/tpg2.70257","article-title":"Pan-NLRome analysis uncovers genetic diversity and evolutionary dynamics among rice, maize and sorghum","volume":"19","author":"Wang","year":"2026","journal-title":"Plant Genome"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1038\/ng.2877","article-title":"Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species","volume":"46","author":"Kim","year":"2014","journal-title":"Nat. Genet."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1307","DOI":"10.1105\/tpc.10.8.1307","article-title":"The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes","volume":"10","author":"Milligan","year":"1998","journal-title":"Plant Cell"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1038\/s41477-020-00834-5","article-title":"Comparative evolutionary genetics of deleterious load in sorghum and maize","volume":"7","author":"Lozano","year":"2021","journal-title":"Nat. Plants"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Jupe, F., Pritchard, L., Etherington, G.J., MacKenzie, K., Cock, P.J.A., Wright, F., Sharma, S.K., Bolser, D., Bryan, G.J., and Jones, J.D.G. (2012). Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genom., 13.","DOI":"10.1186\/1471-2164-13-75"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"814","DOI":"10.1093\/plcell\/koaa002","article-title":"Plant NLR diversity: The known unknowns of pan-NLRomes","volume":"33","author":"Barragan","year":"2020","journal-title":"Plant Cell"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2009","DOI":"10.1105\/tpc.108.060194","article-title":"From Guard to Decoy: A new model for perception of plant pathogen effectors","volume":"20","author":"Kamoun","year":"2008","journal-title":"Plant Cell"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1073\/pnas.0811734106","article-title":"Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation","volume":"106","author":"Parker","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"809","DOI":"10.1105\/tpc.009308","article-title":"Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis","volume":"15","author":"Meyers","year":"2003","journal-title":"Plant Cell"}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/17\/8\/864\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,28]],"date-time":"2026-07-28T04:14:01Z","timestamp":1785212041000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/17\/8\/864"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,7,24]]},"references-count":44,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2026,8]]}},"alternative-id":["genes17080864"],"URL":"https:\/\/doi.org\/10.3390\/genes17080864","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,24]]}}}