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Analysis of the Genome Sequence of Strain GiC-126 of Gloeostereum incarnatum with Genetic Linkage Map

  • Jiang, Wan-Zhu (International Cooperation Research Center of China for New Germplasm Breeding of Edible Mushrooms, Jilin Agricultural University) ;
  • Yao, Fang-Jie (International Cooperation Research Center of China for New Germplasm Breeding of Edible Mushrooms, Jilin Agricultural University) ;
  • Fang, Ming (College of Horticulture, Jilin Agricultural University) ;
  • Lu, Li-Xin (College of Horticulture, Jilin Agricultural University) ;
  • Zhang, You-Min (College of Horticulture, Jilin Agricultural University) ;
  • Wang, Peng (Economic Plants Research Institute, Jilin Academy of Agricultural Sciences) ;
  • Meng, Jing-Jing (College of Horticulture, Jilin Agricultural University) ;
  • Lu, Jia (International Cooperation Research Center of China for New Germplasm Breeding of Edible Mushrooms, Jilin Agricultural University) ;
  • Ma, Xiao-Xu (International Cooperation Research Center of China for New Germplasm Breeding of Edible Mushrooms, Jilin Agricultural University) ;
  • He, Qi (International Cooperation Research Center of China for New Germplasm Breeding of Edible Mushrooms, Jilin Agricultural University) ;
  • Shao, Kai-Sheng (College of Horticulture, Jilin Agricultural University) ;
  • Khan, Asif Ali (International Cooperation Research Center of China for New Germplasm Breeding of Edible Mushrooms, Jilin Agricultural University) ;
  • Wei, Yun-Hui (Institute of Agricultural Applied Microbiology, Jiangxi Academy of Agricultural Sciences)
  • Received : 2021.03.29
  • Accepted : 2021.07.07
  • Published : 2021.08.31

Abstract

Gloeostereum incarnatum has edible and medicinal value and was first cultivated and domesticated in China. We sequenced the G. incarnatum monokaryotic strain GiC-126 on an Illumina HiSeq X Ten system and obtained a 34.52-Mb genome assembly sequence that encoded 16,895 predicted genes. We combined the GiC-126 genome with the published genome of G. incarnatum strain CCMJ2665 to construct a genetic linkage map (GiC-126 genome) that had 10 linkage groups (LGs), and the 15 assembly sequences of CCMJ2665 were integrated into 8 LGs. We identified 1912 simple sequence repeat (SSR) loci and detected 700 genes containing 768 SSRs in the genome; 65 and 100 of them were annotated with gene ontology (GO) terms and KEGG pathways, respectively. Carbohydrate-active enzymes (CAZymes) were identified in 20 fungal genomes and annotated; among them, 144 CAZymes were annotated in the GiC-126 genome. The A mating-type locus (MAT-A) of G. incarnatum was located on scaffold885 at 38.9 cM of LG1 and was flanked by two homeodomain (HD1) genes, mip and beta-fg. Fourteen segregation distortion markers were detected in the genetic linkage map, all of which were skewed toward the parent GiC-126. They formed three segregation distortion regions (SDR1-SDR3), and 22 predictive genes were found in scaffold1920 where three segregation distortion markers were located in SDR1. In this study, we corrected and updated the genomic information of G. incarnatum. Our results will provide a theoretical basis for fine gene mapping, functional gene cloning, and genetic breeding the follow-up of G. incarnatum.

Keywords

Acknowledgement

We thank Margaret Biswas, PhD, from Liwen Bianji, Edanz Editing China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.

References

  1. Li YT, Song H, Li YQ, et al. Study on antioxidant properties of alcohol extract of Gleoeostereum incarnatum fermentation. J Fungal Res. 2010;8: 90-92.
  2. Zhang ZF, Lv GY, Jiang X, et al. Extraction optimization and biological properties of a polysaccharide isolated from Gleoestereum incarnatum. Carbohydr Polym. 2015;117:185-191. https://doi.org/10.1016/j.carbpol.2014.09.059
  3. Wang D, Li Q, Qu YD, et al. The investigation of immunomodulatory activities of Gloeostereum incaratum polysaccharides in cyclophosphamide-induced immunosuppression mice. Exp Ther Med. 2018;15(4):3633-3638.
  4. Li X, Liu X, Zhang YF, et al. Protective effect of Gloeostereum incarnatum on ulcerative colitis via modulation of Nrf2/NF-κB signaling in C57BL/6 mice. Mol Med Rep. 2020;22(4):3418-3428.
  5. Yu Y, Yao FJ, Sun ML, et al. A new Gloeostereum incarnatum cultivar 'Qirou 1. Acta Horticulturae Sin. 2013;40:15-15.
  6. Yu Y, Yao FJ, Zhang YM. A new Gloeostereum incarnatum cultivar 'Jirou 1. Acta Horticulturae Sin. 2016;43:1013-1014.
  7. Gao YL, He D, Wei YY, et al. Research progress on fungal genetic methods. J Fungal Res. 2019;17: 173-179.
  8. Zhang Y, Huang CY, Gao W. Research advances on molecular mushroom breeding. J Fungal Res. 2019;17:229-239.
  9. Wang DD, Li LQ, Ma LY, et al. Progress in development and applications of SSR molecular marker in macrofungi. Microbiology. 2013;40:646-654.
  10. Cao Y, Zhang YZ, Cheng SJ, et al. Genome-wide distributional and comparative analysis of SSR loci in Trametes versicolor. Mycosystema. 2017;36: 1524-1542.
  11. Lu LX, Yao FJ, Wang P, et al. Construction of a genetic linkage map and QTL mapping of agronomic traits in Auricularia auricula-judae. J Microbiol. 2017;55(10):792-799. https://doi.org/10.1007/s12275-017-7241-6
  12. Wang P, Yao FJ, Lu LX, et al. Map-based cloning of genes encoding key enzymes for pigment synthesis in Auricularia cornea. Fungal Biol. 2019; 123(11):843-853. https://doi.org/10.1016/j.funbio.2019.09.002
  13. Yao FJ, Lu LX, Wang P, et al. Development of a molecular marker for fruiting body pattern in Auricularia auricula-judae. Mycobiology. 2018;49: 72-78.
  14. Wang XX, Peng JY, Sun L, et al. Genome sequencing illustrates the genetic basis of the pharmacological properties of Gloeostereum incarnatum. Genes. 2019;10(3):188. https://doi.org/10.3390/genes10030188
  15. Chen SL, Xu J, Liu C, et al. Genome sequence of the model medicinal mushroom Ganoderma lucidum. Nat Commun. 2012;3:913. https://doi.org/10.1038/ncomms1923
  16. Bao DP, Gong M, Zheng HJ, et al. Sequencing and comparative analysis of the straw mushroom (Volvariella volvacea) genome. PLOS One. 2013; 8(3):e58294. https://doi.org/10.1371/journal.pone.0058294
  17. Bau T, Lu T. Advance of macro-fungal genomes Ssquencing. J Fungal Res. 2017;15:151-165.
  18. Au CH, Wong MC, Qin J, et al. Genome sequence and genetic linkage analysis of Shiitake mushroom Lentinula edodes. Nat Prec. 2012. DOI:10.1038/npre.2012.6855.1
  19. Park YJ, Baek JH, Lee S, et al. Whole genome and global gene expression analyses of the model mushroom Flammulina velutipes reveal a high capacity for lignocellulose degradation. PLoS One. 2014;9(4):e93560. https://doi.org/10.1371/journal.pone.0093560
  20. Eid J, Fehr A, Gray J, et al. Real-time DNA sequencing from single polymerase molecules. Science. 2009;323(5910):133-138. https://doi.org/10.1126/science.1162986
  21. Sonnenberg AS, Gao W, Lavrijssen B, et al. A detailed analysis of the recombination landscape of the button mushroom Agaricus bisporus var. bisporus. Fungal Genet Biol. 2016;93:35-45. https://doi.org/10.1016/j.fgb.2016.06.001
  22. Yuan Y, Wu F, Si J, et al. Whole genome sequence of Auricularia heimuer (Basidiomycota, Fungi), the third most important cultivated mushroom worldwide. Genomics. 2019;111:50-58. https://doi.org/10.1016/j.ygeno.2017.12.013
  23. Song H, Yao FJ, Tang J, et al. Research overview of Gloeostereum incarnatum. Chin Edible Fungi. 2008;27:3-4.
  24. Yu Y, Yao FJ, Sun ML, et al. Spring and autumn cultivation management technology of Gloeostereum incarnatum. Northern Horticulture. 2013;10:145-146.
  25. Choi YW, Hyde KD, Ho WWH. Single spore isolation of fungi. Fungal Divers. 1999;3:29-38.
  26. Jiang WZ, Yao FJ, Lu LX, et al. Genetic linkage map construction and quantitative trait loci mapping of agronomic traits in Gloeostereum incarnatum. J Microbiol. 2021;59(1):41-50. https://doi.org/10.1007/s12275-021-0242-5
  27. Watanabe M, Lee K, Goto K, et al. Rapid and effective DNA extraction method with bead grinding for a large amount of fungal DNA. J Food Prot. 2010;73(6):1077-1084. https://doi.org/10.4315/0362-028X-73.6.1077
  28. Borodovsky M, Lomsadze A. Eukaryotic gene prediction using GeneMark.hmm-E and GeneMark-ES. Curr Protocols Bioinform. 2011;4:1-10.
  29. Boeckmann B, Bairoch AM, Apweiler R, et al. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res. 2003;31(1):365-370. https://doi.org/10.1093/nar/gkg095
  30. Ashburner M, Ball CA, Blake JA, et al. Gene ontology: tool for the unification of biology. Nat Genet. 2000;25(1):25-29. https://doi.org/10.1038/75556
  31. Kanehisa M, Goto S, Kawashima S, et al. The KEGG resource for deciphering the genome. Nucleic Acids Res. 2004;32(90001):277D-2280.
  32. Kanehisa M, Goto S, Hattori M, et al. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res. 2006;34(90001): D354-D357. https://doi.org/10.1093/nar/gkj102
  33. Murat C, Riccioni C, Belfiori B, et al. Distribution and localization of microsatellites in the Perigord black truffle genome and identification of new molecular markers. Fungal Genet Biol. 2011;48(6): 592-601. https://doi.org/10.1016/j.fgb.2010.10.007
  34. Untergasser A, Cutcutache I, Koressaar T, et al. Primer3-new capabilities and interfaces. Nucleic Acids Res. 2012;40(15):e115-e115.
  35. Zhang H, Yohe T, Huang L, et al. dbCAN2: A meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2018; 46(W1):W95-W101. https://doi.org/10.1093/nar/gky418
  36. Van Ooijen J, Voorrips R. JoinMap 4.0: Software for the calculation of genetic linkage maps in experimental populations. 2006; Kyazma BV, Wageningen.
  37. Floudas D, Binder D, Riley R, et al. The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science. 2012; 336(6089):1715-1719. https://doi.org/10.1126/science.1221748
  38. Fang M, Wang XE, Chen Y, et al. Genome sequence analysis of Auricularia heimuer combined with genetic linkage map. J Fungi. 2020;6(1):37. https://doi.org/10.3390/jof6010037
  39. Liu DB, Gong J, Dai WK, et al. The genome of Ganderma lucidum provide insights into triterpense biosynthesis and wood degradation. PLos One. 2012;7(5):e36146. https://doi.org/10.1371/journal.pone.0036146
  40. Chen BZ, Gui F, Xie BG, et al. Composition and expression of genes encoding carbohydrate-active enzymes in the straw-degrading mushroom Volvariella volvacea. PLos One. 2013;8(3):e58780. https://doi.org/10.1371/journal.pone.0058780
  41. Qian J, Xu HB, Song JY, et al. Genome-wide analysis of simple sequence repeats in the model medicinal mushroom Ganoderma lucidum. Gene. 2013;512(2):331-336. https://doi.org/10.1016/j.gene.2012.09.127
  42. Wang Y, Chen MJ, Wang H, et al. Microsatellites in the genome of the edible mushroom, Volvariella volvacea. BioMed Res Int. 2014;2014:28912.
  43. Qu JB, Huang CY, Zhang JX. Genome-wide functional analysis of SSR for an edible mushroom Pleurotus ostreatus. Gene. 2016;575(2 Pt 2): 524-530. https://doi.org/10.1016/j.gene.2015.09.027
  44. Lombard V, Golaconda Ramulu H, Drula E, et al. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:D490-D495.
  45. Riley R, Salamov AA, Brown DW, et al. Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci USA. 2014;111(27):9923-9928. https://doi.org/10.1073/pnas.1400592111
  46. James TY, Srivilai P, Kues U, Vilgalys, et al. Evolution of the bipolar mating system of the mushroom Coprinellus disseminatus from its tetrapolar ancestors involves loss of mating-type-specific pheromone receptor function. Genetics. 2006; 172(3):1877-1891. https://doi.org/10.1534/genetics.105.051128
  47. Yi R, Tachikawa T, Mukaiyama H, Mochida, et al. DNA-mediated transformation system in a bipolar basidiomycete, Pholiota microspora (P. nameko). Mycoscience. 2009;50(2):123-129. https://doi.org/10.1007/S10267-008-0456-Y
  48. James TY, Lee M, van Diepen LTA. A Single Mating-Type Locus Composed of Homeodomain genes promotes nuclear migration and heterokaryosis in the white-rot fungus Phanerochaete chrysosporium. Eukaryot Cell. 2011;10(2):249-261. https://doi.org/10.1128/EC.00212-10
  49. Van Peer AF, Park SY, Shin PG, et al. Comparative genomics of the mating-type loci of the mushroom Flammulina velutipes reveals widespread synteny and recent inversions. PLoS One. 2011;6(7):e22249. https://doi.org/10.1371/journal.pone.0022249
  50. Bakkeren G, Kronstad JW. Linkage of mating-type loci distinguishes bipolar from tetrapolar mating in basidiomycetous smut fungi. Proc Natl Acad Sci USA. 1994;91(15):7085-7089. https://doi.org/10.1073/pnas.91.15.7085
  51. Au CH, Wong MC, Bao DP, et al. The genetic structure of the A mating-type locus of Lentinula edodes. Gene. 2014;535(2):184-190. https://doi.org/10.1016/j.gene.2013.11.036
  52. Casselton LA, Asante-Owusu RN, Banham AH, et al. Mating type control of sexual development in Coprinus cinereus. Can J Bot. 1995;73(S1): 266-272. https://doi.org/10.1139/b95-256
  53. Specht CA, Stankis MM, Giasson L, et al. Functional analysis of the homeodomain related proteins of the A alpha locus of Schizophyllum commune. Proc Natl Acad Sci USA. 1992;89(15): 7174-7178. https://doi.org/10.1073/pnas.89.15.7174
  54. Liu HY, Cui JT, Gao YM. Progress of segregation distortion. J Plant Genet Res. 2009;10:613-617.
  55. Liu ZF, Zhu ZP, Huang DR, et al. Genetic analysis on segregation distortion of molecular markers in F2 population of C. Moschata Duch. Mol Plant Breed. 2019;17:3993-3999.