Abstract
Wolfiporia cocos is a saprophytic fungus belonging to the phylum Basidiomycota. The dried sclerotium of this organism has been widely used in traditional Chinese medicine for several thousand years and it is prescribed in many formulations. The W. cocos germplasm resources are complex and diverse, and the molecular mechanisms underlying the growth and development of its sclerotia are unclear. In this study, we used genome resequencing and transcriptome analysis to evaluate the genetic diversity of W. cocos germplasm resources in China and the mechanism of sclerotium growth and development. Phylogenetic and population structure analyses revealed that all the 39 tested strains were divided into three major groups. Most of the strains were clustered into one group, and the remaining strains were clustered into the other two groups. There may be a shared origin of cultivated W. cocos in the main production areas. Transcriptome analysis and quantitative reverse transcription-polymerase chain reaction confirmed that candidate genes related to the yield of W. cocos were mainly enriched in oxidation–reduction and carbohydrate metabolism and highly expressed in the ShenChuan strain, which had the highest comprehensive cultivation score. The findings will be helpful for further understanding the evolution and population structure of W. cocos and determining the functional genes that contribute to the high yield of sclerotia.
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Data Availability
The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: https://www.ncbi.nlm.nih.gov/, PRJNA762230, PRJNA761862.
References
Hattori T, Hayashi K, Nagao T, Furuta K, Ito M, Suzuki Y (1992) Studies on antinephritic effects of plant components (3): effect of pachyman, a main component of Poria cocos Wolf on original-type anti-GBM nephritis in rats and its mechanisms. Jpn J Pharmacol 59:89–96. https://doi.org/10.1254/jjp.59.89
Wang LY, Wan HJ, Chen LX, Zhang HM, Yu ZY (1993) Studies on chemical constituents from solvent extracts of Poria cocos (Schw.) Wolf. Zhongguo Zhong Yao Za Zhi 18:613–639
Kaminaga T, Yasukawa K, Kanno H, Tai T, Nunoura Y, Takido M (1996) Inhibitory effects of lanostane-type triterpene acids, the components of Poria cocos, on tumor promotion by 12-O-tetradecanoylphorbol-13-acetate in two-stage carcinogenesis in mouse skin. Oncology 53:382–385. https://doi.org/10.1159/000227592
Liu XF, Wang XQ, Xu XF, Zhang XW (2019) Purification, antitumor and anti-inflammation activities of an alkali-soluble and carboxymethyl polysaccharide CMP33 from Poria cocos. Int J Biol Macromol 127:39–47. https://doi.org/10.1016/j.ijbiomac.2019.01.029
Shi CY, Ma QH, Ren MY, Liang DD, Yu QT, Luo JB (2017) Antitumorpharmacological mechanism of the oral liquid of Poriacocos polysaccharide. J Ethnopharmacol 209:24–31. https://doi.org/10.1016/j.jep.2017.07.003
Wang NN, Zhang Y, Wang XP, Huang XW, Fei Y, Yu Y, Shou D (2016) Antioxidant property of water-soluble polysaccharides from Poria cocos Wolf using different extraction methods. Int J Biol Macromol 83:103–110. https://doi.org/10.1016/j.ijbiomac.2015.11.032
Baosong C, Sixian W, Gaoqiang L, Li B, Ying H, Ruilin Z, Hongwei L (2020) Anti-inflammatory diterpenes and steroids from peels of the cultivated edible mushroom Wolfiporia cocos. Phytochem Lett 36:11–16. https://doi.org/10.1016/j.phytol.2020.01.005
Feng YL, Cao G, Chen DQ, Vaziri ND, Chen L, Zhang J, Wang M, Guo Y, Zhao YY (2019) Microbiome-metabolomics reveals gut microbiota associated with glycine-conjugated metabolites and polyamine metabolism in chronic kidney disease. Cell Mol Life Sci 76:4961–4978. https://doi.org/10.1007/s00018-019-03155-9
Esteban CI (2009) Medicinal interest of Poria cocos (= Wolfiporia extensa). Rev Iberoam Micol 26:103–107. https://doi.org/10.1016/S1130-1406(09)70019-1
Li L, Wang KQ, Bai J et al (2008) Study on the revulsive cultivation modes of W. cocos. Mod Chin Med 28:16–17. https://doi.org/10.3969/j.issn.1673-4890.2008.12.004
Li L, Wang KQ, Bian YB, Su W, Wang LY (2011) Technical regulations for the production of Hubei W. cocos strains. Mod Chin Med 11:28–32. https://doi.org/10.3969/j.issn.1673-4890.2011.11.007
Xu ZY, Meng H, Xiong H, Bian YB (2014) Biological characteristics of teleomorph and optimized in vitro fruiting conditions of the Hoelen medicinal mushroom, Wolfiporia extensa (Higher Basidiomycetes). Int J Med Mushrooms 16:421–429. https://doi.org/10.1615/intjmedmushrooms.v16.i5.20
Cheng L, Hou J, Wang W, Ding C, Wang Q, Dai J (2015) Investigation and analysis on the production technology of W. cocos in China. Mod Chin Med 3:195–199. https://doi.org/10.13313/j.issn.1673-4890.2015.3.002
Qu Z, Tao G, Zhu GS, Zhu Y, Liu YX, Liu ZY (2008) RAPD analysis of germplasm resources of Wolfiporia cocos. J Fungal Res 6:170–174
Cai DF, Chen MY, Guo ZJ et al (2009) Studies on the biological characteristics of Wolfiporia cocos strain. Edible Fungi China 28:23–26. https://doi.org/10.3969/j.issn.1003-8310.2009.01.009
Luo HM, Qian J, Xu ZC et al (2020) The Wolfiporia cocos genome and transcriptome shed light on the formation of its edible and medicinal Sclerotium. Genom Proteom Bioinform 18:455–467. https://doi.org/10.1016/j.gpb.2019.01.007
Hu BX (2017) De novo assembly and transcriptome analysis of mycelium formed sclerotial and sclerotial development in Wolfiporia cocos. Dissertation. Wuhan Polytechnic University. CNKI:CDMD:2.1018.067545
Cai DF (2013) Selection of fine strain of Wolfiporia cocos for pine stump cultivation. Edible Fungi China 32:14–16
Xu TT, Shen BX, Hu K, Jin CS (2013) Identification and preparation of Anhui Poria cocos spaw. Strait Pharm J 10:18–20. https://doi.org/10.3969/j.issn.1006-3765.2013.10.07t
Wang XX, Wang DQ (2011) Problems and countermeasures of Poria cocos in Jinzhai County of Anhui Province. J Anhui Univ Chin Med 30:60–63. https://doi.org/10.3969/j.issn.1000-2219.2011.03.023
Wang KQ, Yin XR, Huang H, Feng HG, Wang Q, Sun G (2012) Production status and industrialization development countermeasures of Poria in Hubei Province. Mod Chin Med 14:24–27. https://doi.org/10.3969/j.issn.1673-4890.2012.12.007
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303. https://doi.org/10.1101/gr.107524.110
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664. https://doi.org/10.1101/gr.094052.109
Laurentin H, Karlovsky P (2007) AFLP fingerprinting of sesame (Sesamum indicum L.) cultivars: identification, genetic relationship and comparison of AFLP informativeness parameters. Genet Resour Crop Evol 54:1437–1446. https://doi.org/10.1007/s10722-006-9128-y
Qu RZ, Hou L, Lü HL, Li HY (2004) The gene flow of population genetic structure. Yi Chuan 26:377–382. https://doi.org/10.3321/j.issn:0253-9772.2004.03.022
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360. https://doi.org/10.1038/nmeth.3317
Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628. https://doi.org/10.1038/nmeth10.1038/nmeth.1226
Tang WR (2013) Preliminary study on the effects of “bait” on yield and quality of the new Sclerotium in Wolfporia cocos. Dissertation. Huazhong Agricultural University. https://doi.org/10.7666/d.Y2394986
Floudas D, Binder M, Riley R et al (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719. https://doi.org/10.1126/science.1221748
Lu B, Yan J (2003) Sampling strategy for genetic diversity. Biodivers Sci 11:155–161. https://doi.org/10.17520/biods.2003021
Wu SL, Tang SJ, Jin LS, Chen X, Yang YH, Yue L (2018) Quality evaluation and genetic relation identification for different Poria cocos strains. J South Agric 49:8–13
Song Z, Yin Y, Lin Y, Du F, Ren G, Wang Z (2018) The bZIP transcriptional factor activator protein-1 regulates Metarhizium rileyi morphology and mediates microsclerotia formation. Appl Microbiol Biotechnol 102:4577–4588. https://doi.org/10.1007/s00253-018-8941-5
Li B, Tian X, Wang C, Zeng X, Xing Y, Ling H, Yin W, Tian L, Meng Z, Zhang J, Guo S (2017) SWATH label-free proteomics analyses revealed the roles of oxidative stress and antioxidant defensing system in sclerotia formation of Polyporus umbellatus. Sci Rep 7:41283. https://doi.org/10.1038/srep41283
Georgiou CD (1997) Lipid peroxidation in Sclerotium rolfsii: a new look into the mechanism of sclerotial biogenesis in fungi. Mycol Res 101:460–464. https://doi.org/10.1017/S0953756296002882
Liu MM, Xing YM, Zhang DW, Guo SX (2015) Transcriptome analysis of genes involved in defence response in Polyporus umbellatus with Armillaria mellea infection. Sci Rep 5:16075. https://doi.org/10.1038/srep16075
Song C, Liu M, Xing Y, Guo S (2014) ESTs analysis of putative genes engaged in Polyporus umbellatus sclerotial development. Int J Mol Sci 15:15951–15962. https://doi.org/10.3390/ijms150915951
Choi KD, Kwon JK, Shim JO, Lee SS, Lee T, Lee MW (2002) Sclerotial development of Grifola umbellata. Mycobiology 30:65–69. https://doi.org/10.4489/MYCO.2002.30.2.065
Erental A, Dickman MB, Yarden O (2008) Sclerotial development in Sclerotinia sclerotiorum: awakening molecular analysis of a “Dormant” structure. Fungal Biol Rev 22:6–16. https://doi.org/10.1016/j.fbr.2007.10.001
Georgiou CD, Tairis N, Sotiropoulou A (2000) Hydroxyl radical scavengers inhibit lateral-type sclerotial differentiation and growth in phytopathogenic fungi. Mycologia 92:825–834. https://doi.org/10.1080/00275514.2000.12061226
Georgiou CD, Zervoudakis G, Tairis N, Kornaros M (2001) β-carotene production and its role in sclerotial differentiation of Sclerotium rolfsii. Fungal Genet Biol 34:11–20. https://doi.org/10.1006/fgbi.2001.1285
Grabherr MG, Haas BJ, Yassour ML et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883
Feng YL, Lei P, Tian T (2019) Diuretic activity of some fractions of the epidermis of Poria cocos. Ethnopharmacol 150:1114–1118. https://doi.org/10.1016/j.jep.2013.10.043
King BC, Waxman KD, Nenni NV, Walker LP, Bergstrom GC, Gibson DM (2011) Arsenal of plant cell wall degrading enzymes reflects host preference among plant pathogenic fungi. Biotechnol Biofuels 4:4. https://doi.org/10.1186/1754-6834-4-4
Kobira S, Atsumi T, Kakiuchi N, Mikage M (2012) Difference in cultivation characteristics and genetic polymorphism between Chinese and Japanese strains of Wolfiporia cocos Ryvarden et Gilbertson (Poria cocos Wolf). J Nat Med 66:493–499. https://doi.org/10.1007/s11418-011-0612-0
Gan P, Ikeda K, Irieda H, Narusaka M, O’Connell RJ, Narusaka Y, Takano Y, Kubo Y, Shirasu K (2013) Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytol 197:1236–1249. https://doi.org/10.1111/nph.12085
Kubicek CP, Starr TL, Glass NL (2014) Plant cell wall-degrading enzymes and their secretion in plant-pathogenic fungi. Annu Rev Phytopathol 52:427–451. https://doi.org/10.1146/annurev-phyto-102313-045831
Kubo T, Terabayashi S, Takeda S, Sasaki H, Aburada M, Miyamoto KI (2006) Indoor cultivation and cultural characteristics of Wolfiporia cocos sclerotia using mushroom culture bottles. Biol Pharm Bull 29:1191–1196. https://doi.org/10.1248/bpb.29.1191
Barros L, Baptista P, Correia DM, Casal S, Oliveira B, Ferreira I (2007) Fatty acid and sugar compositions, and nutritional value of five wild edible mushrooms from Northeast Portugal. Food Chem 105:140–145. https://doi.org/10.1016/j.foodchem.2007.03.052
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This research was funded by the National Key R&D Programme of China, grant number 2017YFC1703000 and the Hubei Province Technology Innovation Project (General Project), grant number 2020BCB035.
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Conceptualisation, B.-S.H.; data curation, Q.W. and D.L.; formal analysis, Q.W. and H.F.; funding acquisition, B.H.; investigation, Q.W., B.H., and D.L.; methodology, B.H. and H.F.; project administration, H.F.; resources, D.L.; validation, D.L. and Y.M.; writing – review & editing, Q.W., D.L., and Y.M. All authors have read and agreed to the published version of the manuscript.
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Wang, Q., Huang, B., Liu, D. et al. Genome Resequencing and Transcriptome Analysis Reveal the Genetic Diversity of Wolfiporia cocos Germplasm and Genes Related to High Yield. Curr Microbiol 79, 312 (2022). https://doi.org/10.1007/s00284-022-03011-3
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DOI: https://doi.org/10.1007/s00284-022-03011-3