1887

Abstract

Understanding the genomic diversity and functional implications of species is crucial for elucidating their evolutionary history and biotechnological potential. Here, we present the first pan-genomic analysis of spp., combining five newly sequenced genomes with ten publicly available genomes. Our comprehensive comparative study unveiled a rich genomic landscape, identifying core genes shared among all strains and species-specific gene sets. Additionally, we identified structural variants impacting the expression of key genes, including insights into the gene involved in DNA repair and recombination processes, which exhibits a 440 bp insertion in the promoter region and a leucine-to-serine mutation in the gene body, potentially increasing spore production in the S3 strain. Overall, our study provides valuable insights into the genomic architecture and functional diversity of , paving the way for further research on its evolutionary dynamics, biotechnological applications and pharmaceutical potential.

Funding
This study was supported by the:
  • School management project of Fujian University of Traditional Chinese Medicine (Award X2021001)
    • Principle Award Recipient: XiaoyanLi
  • School management project of Fujian University of Traditional Chinese Medicine (Award XJC2023011)
    • Principle Award Recipient: WenXu
  • Science and Technology Planning Project of Fuzhou (Award 2023-P-005)
    • Principle Award Recipient: ZehaoHuang
  • Fujian Provincial Department of Science and Technology (Award 2022Y4017)
    • Principle Award Recipient: YuLin
  • National Key R&D Program of China (Award 2019YFC1710505)
    • Principle Award Recipient: YuLin
  • State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources (Award SKLCUSA-b202302)
    • Principle Award Recipient: HaifengWang
  • Sugarcane Research Foundation of Guangxi University (Award 2022GZA002)
    • Principle Award Recipient: HaifengWang
  • Natural Science Foundation of Guangxi Zhuang Autonomous Region (Award 2023GXNSFDA026034)
    • Principle Award Recipient: HaifengWang
  • National Natural Science Foundation of China (Award 32160142)
    • Principle Award Recipient: HaifengWang
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2024-11-20
2024-12-09
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References

  1. Da J, Wu W-Y, Hou J-J, Long H-L, Yao S et al. Comparison of two officinal Chinese pharmacopoeia species of Ganoderma based on chemical research with multiple technologies and chemometrics analysis. J Chromatogr A 2012; 1222:59–70 [View Article] [PubMed]
    [Google Scholar]
  2. Xu J, Li P. Researches and application of ganoderma spores powder. In Ganoderma and Health: Biology, Chemistry and Industry 2019 pp 157–186 [View Article]
    [Google Scholar]
  3. Zhang W, Tao J, Yang X, Yang Z, Zhang L et al. Antiviral effects of two Ganoderma lucidum triterpenoids against enterovirus 71 infection. Biochem Biophys Res Commun 2014; 449:307–312 [View Article] [PubMed]
    [Google Scholar]
  4. Akihisa T, Nakamura Y, Tagata M, Tokuda H, Yasukawa K et al. Anti‐inflammatory and anti‐tumor‐promoting effects of triterpene acids and sterols from the fungus Ganoderma lucidum. Chem Biodivers 2007; 4:224–231 [View Article]
    [Google Scholar]
  5. Chen S, Xu J, Liu C, Zhu Y, Nelson DR et al. Genome sequence of the model medicinal mushroom Ganoderma lucidum. Nat Commun 2012; 3:913 [View Article] [PubMed]
    [Google Scholar]
  6. Jiang N, Li Z, Dai Y, Liu Z, Han X et al. Massive genome investigations reveal insights of prevalent introgression for environmental adaptation and triterpene biosynthesis in Ganoderma. Mol Ecol Resour 2022 [View Article] [PubMed]
    [Google Scholar]
  7. Saxena RK, Edwards D, Varshney RK. Structural variations in plant genomes. Brief Funct Genom 2014; 13:296–307 [View Article] [PubMed]
    [Google Scholar]
  8. Lye ZN, Purugganan MD. Copy number variation in domestication. Trends Plant Sci 2019; 24:352–365 [View Article] [PubMed]
    [Google Scholar]
  9. Lam H-M, Xu X, Liu X, Chen W, Yang G et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet 2010; 42:1053–1059 [View Article] [PubMed]
    [Google Scholar]
  10. Bayer PE, Golicz AA, Scheben A, Batley J, Edwards D. Plant pan-genomes are the new reference. Nat Plants 2020; 6:914–920 [View Article] [PubMed]
    [Google Scholar]
  11. Liu Y, Du H, Li P, Shen Y, Peng H et al. Pan-genome of wild and cultivated soybeans. Cell 2020; 182:162–176 [View Article] [PubMed]
    [Google Scholar]
  12. Wang B, Hou M, Shi J, Ku L, Song W et al. De novo genome assembly and analyses of 12 founder inbred lines provide insights into maize heterosis. Nat Genet 2023; 55:312–323 [View Article] [PubMed]
    [Google Scholar]
  13. Li N, He Q, Wang J, Wang B, Zhao J et al. Super-pangenome analyses highlight genomic diversity and structural variation across wild and cultivated tomato species. Nat Genet 2023; 55:852–860 [View Article] [PubMed]
    [Google Scholar]
  14. Qin P, Lu H, Du H, Wang H, Chen W et al. Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations. Cell 2021; 184:3542–3558 [View Article] [PubMed]
    [Google Scholar]
  15. Jayakodi M, Padmarasu S, Haberer G, Bonthala VS, Gundlach H et al. The barley pan-genome reveals the hidden legacy of mutation breeding. Nature 2020; 588:284–289 [View Article] [PubMed]
    [Google Scholar]
  16. Danilevicz MF, Tay Fernandez CG, Marsh JI, Bayer PE, Edwards D. Plant pangenomics: approaches, applications and advancements. Curr Opin Plant Biol 2020; 54:18–25 [View Article] [PubMed]
    [Google Scholar]
  17. Marçais G, Kingsford C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 2011; 27:764–770 [View Article] [PubMed]
    [Google Scholar]
  18. Vurture GW, Sedlazeck FJ, Nattestad M, Underwood CJ, Fang H et al. GenomeScope: fast reference-free genome profiling from short reads. Bioinformatics 2017; 33:2202–2204 [View Article] [PubMed]
    [Google Scholar]
  19. Cheng H, Concepcion GT, Feng X, Zhang H, Li H. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat Methods 2021; 18:170–175 [View Article] [PubMed]
    [Google Scholar]
  20. Roach MJ, Schmidt SA, Borneman AR. Purge haplotigs: allelic contig reassignment for third-gen diploid genome assemblies. BMC Bioinform 2018; 19:460 [View Article] [PubMed]
    [Google Scholar]
  21. Alonge M, Lebeigle L, Kirsche M, Jenike K, Ou S et al. Automated assembly scaffolding using RagTag elevates a new tomato system for high-throughput genome editing. Genome Biol 2022; 23:258 [View Article] [PubMed]
    [Google Scholar]
  22. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
    [Google Scholar]
  23. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 2015; 31:3210–3212 [View Article] [PubMed]
    [Google Scholar]
  24. Jung Y, Han D. BWA-MEME: BWA-MEM emulated with a machine learning approach. Bioinformatics 2022; 38:2404–2413 [View Article] [PubMed]
    [Google Scholar]
  25. Flynn JM, Hubley R, Goubert C, Rosen J, Clark AG et al. RepeatModeler2 for automated genomic discovery of transposable element families. Proc Natl Acad Sci U S A 2020; 117:9451–9457 [View Article] [PubMed]
    [Google Scholar]
  26. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O et al. Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 2005; 110:462–467 [View Article] [PubMed]
    [Google Scholar]
  27. Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 2019; 47:D309–D314 [View Article] [PubMed]
    [Google Scholar]
  28. Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 2019; 20:238 [View Article] [PubMed]
    [Google Scholar]
  29. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019; 35:4453–4455 [View Article] [PubMed]
    [Google Scholar]
  30. Edgar RC. MUSCLE v5 enables improved estimates of phylogenetic tree confidence by ensemble bootstrapping. BioRxiv 20212021
    [Google Scholar]
  31. Sanderson MJ. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 2003; 19:301–302 [View Article]
    [Google Scholar]
  32. De Bie T, Cristianini N, Demuth JP, Hahn MW. CAFE: a computational tool for the study of gene family evolution. Bioinformatics 2006; 22:1269–1271 [View Article] [PubMed]
    [Google Scholar]
  33. Goel M, Sun H, Jiao WB, Schneeberger K. SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies. Genome Biol 2019; 20:277 [View Article] [PubMed]
    [Google Scholar]
  34. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 2012; 6:80–92 [View Article] [PubMed]
    [Google Scholar]
  35. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  36. Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol 2019; 37:907–915 [View Article] [PubMed]
    [Google Scholar]
  37. Kovaka S, Zimin AV, Pertea GM, Razaghi R, Salzberg SL et al. Transcriptome assembly from long-read RNA-seq alignments with StringTie2. Genome Biol 2019; 20:278 [View Article] [PubMed]
    [Google Scholar]
  38. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014; 15:550 [View Article] [PubMed]
    [Google Scholar]
  39. Klopfenstein DV, Zhang L, Pedersen BS, Ramírez F, Warwick Vesztrocy A et al. GOATOOLS: a python library for gene ontology analyses. Sci Rep 2018; 8:10872 [View Article] [PubMed]
    [Google Scholar]
  40. Liu D, Gong J, Dai W, Kang X, Huang Z et al. The genome of Ganderma lucidum provide insights into triterpense biosynthesis and wood degradation. PLoS One 2012; 7:e36146 [View Article]
    [Google Scholar]
  41. Couturier M, Navarro D, Chevret D, Henrissat B, Piumi F et al. Enhanced degradation of softwood versus hardwood by the white-rot fungus Pycnoporus coccineus. Biotechnol Biofuels 2015; 8:216 [View Article] [PubMed]
    [Google Scholar]
  42. Eastwood DC, Floudas D, Binder M, Majcherczyk A, Schneider P et al. The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science 2011; 333:762–765 [View Article] [PubMed]
    [Google Scholar]
  43. Floudas D, Binder M, Riley R, Barry K, Blanchette RA et al. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 2012; 336:1715–1719 [View Article] [PubMed]
    [Google Scholar]
  44. Martin F, Aerts A, Ahrén D, Brun A, Danchin EGJ et al. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 2008; 452:88–92 [View Article] [PubMed]
    [Google Scholar]
  45. Stajich JE, Wilke SK, Ahrén D, Au CH, Birren BW et al. Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc Natl Acad Sci U S A 2010; 107:11889–11894 [View Article] [PubMed]
    [Google Scholar]
  46. Yao Y-J, Wang X-C, Wang B. Epitypification of Ganoderma sichuanense JD Zhao & XQ Zhang (Ganodermataceae). Taxon 2013; 62:1025–1031
    [Google Scholar]
  47. Hou X, Wang D, Cheng Z, Wang Y, Jiao Y. A near-complete assembly of an Arabidopsis thaliana genome. Mol Plant 2022; 15:1247–1250 [View Article] [PubMed]
    [Google Scholar]
  48. Song J-M, Xie W-Z, Wang S, Guo Y-X, Koo D-H et al. Two gap-free reference genomes and a global view of the centromere architecture in rice. Mol Plant 2021; 14:1757–1767 [View Article] [PubMed]
    [Google Scholar]
  49. Huang Y, He J, Xu Y, Zheng W, Wang S et al. Pangenome analysis provides insight into the evolution of the orange subfamily and a key gene for citric acid accumulation in citrus fruits. Nat Genet 2023; 55:1964–1975 [View Article] [PubMed]
    [Google Scholar]
  50. Li K, Na K, Sang T, Wu K, Wang Y et al. The ethanol extracts of sporoderm-broken spores of Ganoderma lucidum inhibit colorectal cancer in vitro and in vivo. Oncol Rep 2017; 38:2803–2813 [View Article] [PubMed]
    [Google Scholar]
  51. Na K, Li K, Sang T, Wu K, Wang Y et al. Anticarcinogenic effects of water extract of sporoderm-broken spores of Ganoderma lucidum on colorectal cancer in vitro and in vivo. Int J Oncol 2017; 50:1541–1554 [View Article]
    [Google Scholar]
  52. Cai M, Tan Z, Wu X, Liang X, Liu Y et al. Comparative transcriptome analysis of genes and metabolic pathways involved in sporulation in Ganoderma lingzhi. G3 (Bethesda) 2022; 12:jkab448 [View Article] [PubMed]
    [Google Scholar]
  53. Lavrijssen B, Baars JP, Lugones LG, Scholtmeijer K, Sedaghat Telgerd N et al. Interruption of an MSH4 homolog blocks meiosis in metaphase I and eliminates spore formation in Pleurotus ostreatus. PLoS One 2020; 15:e0241749 [View Article] [PubMed]
    [Google Scholar]
  54. Mathur M, Mathur P. Prediction of global distribution of Ganoderma lucidum (Leys.) Karsten: a machine learning maxent analysis for a commercially important plant fungus. Indian J Ecol 2023; 50:289–305
    [Google Scholar]
  55. Okuda Y, Murakami S, Honda Y, Matsumoto T. An MSH4 homolog, stpp1, from Pleurotus pulmonarius is a “silver bullet” for resolving problems caused by spores in cultivated mushrooms. Appl Environ Microbiol 2013; 79:4520–4527 [View Article] [PubMed]
    [Google Scholar]
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