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ASFV transcription is particularly complex because of its unique host-independent transcription system. Using nanopore sequencing technology, we accurately identified the viral transcription start and termination sites. Combining direct RNA sequencing with experimental verification strongly supports the presence of long multicistronic RNAs. By combining this information with the viral genome annotation, we identified six novel transcriptional genes with potential functions. Furthermore, we observed transcriptional \u201cread-through\u201d events, in which transcription initiated at a common start site continues beyond typical termination sites, producing multiple RNA transcripts of different lengths. Additionally, via direct RNA nanopore sequencing, we identified m6A and m5C methylation modifications on viral transcripts, which are predominantly distributed at both termini of the viral genome. Compared to unmodified transcripts, modified RNAs have shorter poly(A) tails, indicating a correlation between RNA modification and poly(A) tail length. Further investigation of ASFV transcriptional architecture, \u201cread-through\u201d events, RNA modifications, and candidate genes may improve our understanding of the viral life cycle and pathogenicity and inform the identification of potential antiviral targets.<\/jats:p>","DOI":"10.1371\/journal.ppat.1014617","type":"journal-article","created":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T17:46:56Z","timestamp":1790185616000},"page":"e1014617","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["Transcriptional architecture of African swine fever virus"],"prefix":"10.1371","volume":"22","author":[{"given":"Guiqian","family":"Wang","sequence":"first","affiliation":[{"name":"National Key Laboratory of Agricultural Microbiology, Hainan Research Institute, Hubei Hongshan Laboratory, College of Animal Sciences & Technology and College of Veterinary Medicine, Huazhong Agricultural University","place":["Wuhan, Hubei, China"]},{"name":"Key Laboratory of Preventive Veterinary Medicine in Hubei Province, The Cooperative Innovation Centre for Sustainable Pig Production","place":["Wuhan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pengfei","family":"Li","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Agricultural Microbiology, Hainan Research Institute, Hubei Hongshan Laboratory, College of Animal Sciences & Technology and College of Veterinary Medicine, Huazhong Agricultural University","place":["Wuhan, Hubei, China"]},{"name":"Key Laboratory of Preventive Veterinary Medicine in Hubei Province, The Cooperative Innovation Centre for Sustainable Pig Production","place":["Wuhan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinglin","family":"He","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Agricultural Microbiology, Hainan Research Institute, Hubei Hongshan Laboratory, College of Animal Sciences & Technology and College of Veterinary Medicine, Huazhong Agricultural University","place":["Wuhan, Hubei, China"]},{"name":"Key Laboratory of Preventive Veterinary Medicine in Hubei Province, The Cooperative Innovation Centre for Sustainable Pig Production","place":["Wuhan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hua","family":"Cao","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Agricultural Microbiology, Hainan Research Institute, Hubei Hongshan Laboratory, College of Animal Sciences & Technology and College of Veterinary Medicine, Huazhong Agricultural University","place":["Wuhan, Hubei, China"]},{"name":"Key Laboratory of Preventive Veterinary Medicine in Hubei Province, The Cooperative Innovation Centre for Sustainable Pig Production","place":["Wuhan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ahmed","family":"H. 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