{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,31]],"date-time":"2026-05-31T13:00:34Z","timestamp":1780232434646,"version":"3.54.0"},"reference-count":89,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2026,2,28]],"date-time":"2026-02-28T00:00:00Z","timestamp":1772236800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Young Scientist Fostering Funds for the National Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops and the Fundamental Research Funds for the Central Universities, China","award":["2662024SZ002"],"award-info":[{"award-number":["2662024SZ002"]}]},{"name":"National Natural Science Fund for Excellent Young Scientists Fund Program"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,5,5]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Citrus species are economically and nutritionally vital, with their fruits cultivated globally. Despite the publication of multiple genomes for Citrus, high-quality assemblies that achieve both haplotype resolution and telomere-to-telomere (HR-T2T) continuity remain scarce\u2014pummelo (Citrus maxima) being a notable example. Compounded by limitations in gene annotation quality, these gaps hinder functional genomic research and genomics-assisted breeding. Here, we report the first high-quality HR\u2013T2T genome assembly of pummelo, generated using PacBio HiFi and Oxford Nanopore sequencing. The two haplotype assemblies presented contig N50 values of 38.58 and 32.57\u00a0Mb, completeness scores of 99.36% and 99.66%, and nucleotide accuracies of 99.99994% and 99.99997%, respectively. We developed HapGene, a haplotype-aware annotation pipeline that integrates short-read RNA-Seq and long-read Iso-Seq data to enable unbiased annotation. Benchmarking showed HapGene captured 3% to 10% of genes missed or misannotated by conventional pipelines and reduces false haplotype-specific genes by 4- to 5-fold. Leveraging 380 Gb of newly sequenced and 2792 Gb of public transcriptomic data, we comprehensively annotated protein-coding and non-coding genes across three major Citrus crops (sweet orange, pummelo, and mandarin). This effort revealed 18\u2009757\u201321\u2009083 alternative splicing events, 1725\u20131853 resistance gene analogues, and 2392\u20133757 long intergenic RNAs (lincRNAs). Genomic and transcriptomic characterization of lincRNAs indicated their functional innovation (many associated with stress responses) in Citrus. Additionally, we revealed around one-third of genes exhibited tissue-specific allelic differential expression. Our work provides a critical genomic resource and analytical tool to advance Citrus genomic research, thereby driving progress in functional and evolutionary genomics while laying a robust foundation for precise genomics-assisted breeding.<\/jats:p>","DOI":"10.1093\/hr\/uhag048","type":"journal-article","created":{"date-parts":[[2026,2,28]],"date-time":"2026-02-28T05:31:54Z","timestamp":1772256714000},"source":"Crossref","is-referenced-by-count":1,"title":["Haplotype-resolved telomere-to-telomere assembly and haplotype-aware annotation pipeline enable high-quality reannotation of three\n                    <i>Citrus<\/i>\n                    genomes"],"prefix":"10.1093","volume":"13","author":[{"given":"Jing","family":"Huang","sequence":"first","affiliation":[{"name":"National Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, Huazhong Agricultural University , Wuhan 430070 ,","place":["China"]},{"name":"Hubei Hongshan Laboratory , Wuhan 430070 ,","place":["China"]},{"name":"Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University , Wuhan 430070 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pei-Xuan","family":"Xiao","sequence":"additional","affiliation":[{"name":"National Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, Huazhong Agricultural University , Wuhan 430070 ,","place":["China"]},{"name":"Hubei Hongshan Laboratory , Wuhan 430070 ,","place":["China"]},{"name":"Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University , Wuhan 430070 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ling","family":"Cui","sequence":"additional","affiliation":[{"name":"National Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, Huazhong Agricultural University , Wuhan 430070 ,","place":["China"]},{"name":"Hubei Hongshan Laboratory , Wuhan 430070 ,","place":["China"]},{"name":"Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University , Wuhan 430070 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lei","family":"Tan","sequence":"additional","affiliation":[{"name":"National Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, Huazhong Agricultural University , Wuhan 430070 ,","place":["China"]},{"name":"Hubei Hongshan Laboratory , Wuhan 430070 ,","place":["China"]},{"name":"Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University , Wuhan 430070 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shenchao","family":"Zhu","sequence":"additional","affiliation":[{"name":"National Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, Huazhong Agricultural University , Wuhan 430070 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2976-7585","authenticated-orcid":false,"given":"Junli","family":"Ye","sequence":"additional","affiliation":[{"name":"National Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, Huazhong Agricultural University , Wuhan 430070 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8355-2959","authenticated-orcid":false,"given":"Wen-Biao","family":"Jiao","sequence":"additional","affiliation":[{"name":"National Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, Huazhong Agricultural University , Wuhan 430070 ,","place":["China"]},{"name":"Hubei Hongshan Laboratory , Wuhan 430070 ,","place":["China"]},{"name":"Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University , Wuhan 430070 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2026,2,28]]},"reference":[{"key":"2026053108114317100_ref1","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1038\/nbt.2906","article-title":"Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication","volume":"32","author":"Wu","year":"2014","journal-title":"Nat Biotechnol"},{"key":"2026053108114317100_ref2","doi-asserted-by":"crossref","DOI":"10.1016\/j.xplc.2020.100138","article-title":"Genomic insights into citrus domestication and its important agronomic traits","volume":"2","author":"Rao","year":"2021","journal-title":"Plant Commun"},{"key":"2026053108114317100_ref3","doi-asserted-by":"crossref","first-page":"369","DOI":"10.2307\/2484763","article-title":"On the history and origin of citrus","volume":"102","author":"Scora","year":"1975","journal-title":"B Torrey Bot Club"},{"key":"2026053108114317100_ref4","doi-asserted-by":"crossref","first-page":"1806","DOI":"10.1016\/j.molp.2025.08.014","article-title":"Designing better crops with phased pangenomes","volume":"18","author":"Lian","year":"2025","journal-title":"Mol Plant"},{"key":"2026053108114317100_ref5","doi-asserted-by":"crossref","first-page":"1018","DOI":"10.1038\/s41588-020-0699-x","article-title":"Haplotype-resolved genome analyses of a heterozygous diploid potato","volume":"52","author":"Zhou","year":"2020","journal-title":"Nat Genet"},{"key":"2026053108114317100_ref6","doi-asserted-by":"crossref","first-page":"1423","DOI":"10.1038\/s41588-020-00723-9","article-title":"Phased diploid genome assemblies and pan-genomes provide insights into the genetic history of apple domestication","volume":"52","author":"Sun","year":"2020","journal-title":"Nat Genet"},{"key":"2026053108114317100_ref7","doi-asserted-by":"crossref","first-page":"2494","DOI":"10.1038\/s41467-020-16338-x","article-title":"Allele-aware chromosome-level genome assembly and efficient transgene-free genome editing for the autotetraploid cultivated alfalfa","volume":"11","author":"Chen","year":"2020","journal-title":"Nat Commun"},{"key":"2026053108114317100_ref8","doi-asserted-by":"crossref","first-page":"uhaf033","DOI":"10.1093\/hr\/uhaf033","article-title":"Citrus genomes: past, present and future","volume":"12","author":"Nakandala","year":"2025","journal-title":"Hortic Res"},{"key":"2026053108114317100_ref9","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1038\/nature25447","article-title":"Genomics of the origin and evolution of Citrus","volume":"554","author":"Wu","year":"2018","journal-title":"Nature"},{"key":"2026053108114317100_ref10","doi-asserted-by":"crossref","first-page":"1964","DOI":"10.1038\/s41588-023-01516-6","article-title":"Pangenome analysis provides insight into the evolution of the orange subfamily and a key gene for citric acid accumulation in citrus fruits","volume":"55","author":"Huang","year":"2023","journal-title":"Nat Genet"},{"key":"2026053108114317100_ref11","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1186\/s13059-025-03817-x","article-title":"Pan-S-locus analysis reveals insights into the origin and evolution of self-incompatibility in the orange subfamily","volume":"26","author":"Hu","year":"2025","journal-title":"Genome Biol"},{"key":"2026053108114317100_ref12","doi-asserted-by":"crossref","first-page":"754","DOI":"10.1038\/s41588-025-02122-4","article-title":"Origin and de novo domestication of sweet orange","volume":"57","author":"Liu","year":"2025","journal-title":"Nat Genet"},{"key":"2026053108114317100_ref13","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1038\/ng.3839","article-title":"Genomic analyses of primitive, wild and cultivated citrus provide insights into asexual reproduction","volume":"49","author":"Wang","year":"2017","journal-title":"Nat Genet"},{"key":"2026053108114317100_ref14","doi-asserted-by":"crossref","first-page":"uhac175","DOI":"10.1093\/hr\/uhac175","article-title":"The high-quality genome of pummelo provides insights into the tissue-specific regulation of citric acid and anthocyanin during domestication","volume":"9","author":"Lu","year":"2022","journal-title":"Hortic Res"},{"key":"2026053108114317100_ref15","doi-asserted-by":"crossref","first-page":"1577","DOI":"10.1111\/pbi.14058","article-title":"Evolution-guided multiomics provide insights into the strengthening of bioactive flavone biosynthesis in medicinal pummelo","volume":"21","author":"Zheng","year":"2023","journal-title":"Plant Biotechnol J"},{"key":"2026053108114317100_ref16","doi-asserted-by":"crossref","first-page":"3083","DOI":"10.1111\/pbi.70111","article-title":"CgABR1 - CgFAD negatively regulates the fruit neck length in 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