The golden genome annotation of Ganoderma lingzhi reveals a more complex scenario of eukaryotic gene structure and transcription activity
Abstract Background It is generally accepted that nuclear genes in eukaryotes are located independently on chromosomes and expressed in a monocistronic manner. However, accumulating evidence suggests a more complex landscape of gene structure and transcription. Ganoderma lingzhi, a model medicinal f...
Saved in:
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2024-11-01
|
| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-024-02073-y |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850064537632374784 |
|---|---|
| author | Lining Wang Peiqi Shi Zhaohua Ping Qinghua Huang Liqun Jiang Nianfang Ma Qingfu Wang Jiang Xu Yajie Zou Zhihai Huang |
| author_facet | Lining Wang Peiqi Shi Zhaohua Ping Qinghua Huang Liqun Jiang Nianfang Ma Qingfu Wang Jiang Xu Yajie Zou Zhihai Huang |
| author_sort | Lining Wang |
| collection | DOAJ |
| description | Abstract Background It is generally accepted that nuclear genes in eukaryotes are located independently on chromosomes and expressed in a monocistronic manner. However, accumulating evidence suggests a more complex landscape of gene structure and transcription. Ganoderma lingzhi, a model medicinal fungus, currently lacks high-quality genome annotation, hindering genetic studies. Results Here, we reported a golden annotation of G. lingzhi, featuring 14,147 high-confidence genes derived from extensive manual corrections. Novel characteristics of gene structure and transcription were identified accordingly. Notably, non-canonical splicing sites accounted for 1.99% of the whole genome, with the predominant types being GC-AG (1.85%), GT-AC (0.05%), and GT-GG (0.04%). 1165 pairs of genes were found to have overlapped transcribed regions, and 92.19% of which showed opposite directions of gene transcription. A total of 5,412,158 genetic variations were identified among 13 G. lingzhi strains, and the manually corrected gene sets resulted in enhanced functional annotation of these variations. More than 60% of G. lingzhi genes were alternatively spliced. In addition, we found that two or more protein-coding genes (PCGs) can be transcribed into a single RNA molecule, referred to as polycistronic genes. In total, 1272 polycistronic genes associated with 2815 PCGs were identified. Conclusions The widespread presence of polycistronic genes in G. lingzhi strongly complements the theory that polycistron is also present in eukaryotic genomes. The extraordinary gene structure and transcriptional activity uncovered through this golden annotation provide implications for the study of genes, genomes, and related studies in G. lingzhi and other eukaryotes. |
| format | Article |
| id | doaj-art-e5f079b162334b128c06266b55d17d40 |
| institution | DOAJ |
| issn | 1741-7007 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj-art-e5f079b162334b128c06266b55d17d402025-08-20T02:49:16ZengBMCBMC Biology1741-70072024-11-0122111610.1186/s12915-024-02073-yThe golden genome annotation of Ganoderma lingzhi reveals a more complex scenario of eukaryotic gene structure and transcription activityLining Wang0Peiqi Shi1Zhaohua Ping2Qinghua Huang3Liqun Jiang4Nianfang Ma5Qingfu Wang6Jiang Xu7Yajie Zou8Zhihai Huang9Guangdong Engineering Laboratory of Biomass Value-added Utilization, Guangdong Engineering Research & Development Center for Comprehensive Utilization of Plant Fiber, Guangzhou Key Laboratory for Comprehensive Utilization of Plant Fiber, Institute of Biological and Medical Engineering, Guangdong Academy of SciencesThe Second Clinical College, Guangzhou University of Chinese MedicineGuangdong Engineering Laboratory of Biomass Value-added Utilization, Guangdong Engineering Research & Development Center for Comprehensive Utilization of Plant Fiber, Guangzhou Key Laboratory for Comprehensive Utilization of Plant Fiber, Institute of Biological and Medical Engineering, Guangdong Academy of SciencesGuangdong Engineering Laboratory of Biomass Value-added Utilization, Guangdong Engineering Research & Development Center for Comprehensive Utilization of Plant Fiber, Guangzhou Key Laboratory for Comprehensive Utilization of Plant Fiber, Institute of Biological and Medical Engineering, Guangdong Academy of SciencesGuangdong Engineering Laboratory of Biomass Value-added Utilization, Guangdong Engineering Research & Development Center for Comprehensive Utilization of Plant Fiber, Guangzhou Key Laboratory for Comprehensive Utilization of Plant Fiber, Institute of Biological and Medical Engineering, Guangdong Academy of SciencesGuangdong Engineering Laboratory of Biomass Value-added Utilization, Guangdong Engineering Research & Development Center for Comprehensive Utilization of Plant Fiber, Guangzhou Key Laboratory for Comprehensive Utilization of Plant Fiber, Institute of Biological and Medical Engineering, Guangdong Academy of SciencesGuangdong Engineering Laboratory of Biomass Value-added Utilization, Guangdong Engineering Research & Development Center for Comprehensive Utilization of Plant Fiber, Guangzhou Key Laboratory for Comprehensive Utilization of Plant Fiber, Institute of Biological and Medical Engineering, Guangdong Academy of SciencesInstitute of Chinese Materia Medica, China Academy of Chinese Medical SciencesInstitute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesThe Second Clinical College, Guangzhou University of Chinese MedicineAbstract Background It is generally accepted that nuclear genes in eukaryotes are located independently on chromosomes and expressed in a monocistronic manner. However, accumulating evidence suggests a more complex landscape of gene structure and transcription. Ganoderma lingzhi, a model medicinal fungus, currently lacks high-quality genome annotation, hindering genetic studies. Results Here, we reported a golden annotation of G. lingzhi, featuring 14,147 high-confidence genes derived from extensive manual corrections. Novel characteristics of gene structure and transcription were identified accordingly. Notably, non-canonical splicing sites accounted for 1.99% of the whole genome, with the predominant types being GC-AG (1.85%), GT-AC (0.05%), and GT-GG (0.04%). 1165 pairs of genes were found to have overlapped transcribed regions, and 92.19% of which showed opposite directions of gene transcription. A total of 5,412,158 genetic variations were identified among 13 G. lingzhi strains, and the manually corrected gene sets resulted in enhanced functional annotation of these variations. More than 60% of G. lingzhi genes were alternatively spliced. In addition, we found that two or more protein-coding genes (PCGs) can be transcribed into a single RNA molecule, referred to as polycistronic genes. In total, 1272 polycistronic genes associated with 2815 PCGs were identified. Conclusions The widespread presence of polycistronic genes in G. lingzhi strongly complements the theory that polycistron is also present in eukaryotic genomes. The extraordinary gene structure and transcriptional activity uncovered through this golden annotation provide implications for the study of genes, genomes, and related studies in G. lingzhi and other eukaryotes.https://doi.org/10.1186/s12915-024-02073-yG. lingzhiNon-canonical splicing sitesOverlapped genesAlternative splicingEukaryotic polycistronic genes |
| spellingShingle | Lining Wang Peiqi Shi Zhaohua Ping Qinghua Huang Liqun Jiang Nianfang Ma Qingfu Wang Jiang Xu Yajie Zou Zhihai Huang The golden genome annotation of Ganoderma lingzhi reveals a more complex scenario of eukaryotic gene structure and transcription activity BMC Biology G. lingzhi Non-canonical splicing sites Overlapped genes Alternative splicing Eukaryotic polycistronic genes |
| title | The golden genome annotation of Ganoderma lingzhi reveals a more complex scenario of eukaryotic gene structure and transcription activity |
| title_full | The golden genome annotation of Ganoderma lingzhi reveals a more complex scenario of eukaryotic gene structure and transcription activity |
| title_fullStr | The golden genome annotation of Ganoderma lingzhi reveals a more complex scenario of eukaryotic gene structure and transcription activity |
| title_full_unstemmed | The golden genome annotation of Ganoderma lingzhi reveals a more complex scenario of eukaryotic gene structure and transcription activity |
| title_short | The golden genome annotation of Ganoderma lingzhi reveals a more complex scenario of eukaryotic gene structure and transcription activity |
| title_sort | golden genome annotation of ganoderma lingzhi reveals a more complex scenario of eukaryotic gene structure and transcription activity |
| topic | G. lingzhi Non-canonical splicing sites Overlapped genes Alternative splicing Eukaryotic polycistronic genes |
| url | https://doi.org/10.1186/s12915-024-02073-y |
| work_keys_str_mv | AT liningwang thegoldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT peiqishi thegoldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT zhaohuaping thegoldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT qinghuahuang thegoldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT liqunjiang thegoldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT nianfangma thegoldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT qingfuwang thegoldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT jiangxu thegoldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT yajiezou thegoldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT zhihaihuang thegoldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT liningwang goldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT peiqishi goldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT zhaohuaping goldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT qinghuahuang goldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT liqunjiang goldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT nianfangma goldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT qingfuwang goldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT jiangxu goldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT yajiezou goldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity AT zhihaihuang goldengenomeannotationofganodermalingzhirevealsamorecomplexscenarioofeukaryoticgenestructureandtranscriptionactivity |