Abstract
Wolfiporia cocos is an important medicinal and edible fungus that grows in association with pine trees, and its dried sclerotium has been used as a traditional medicine in China for centuries. However, the commercial production of W. cocos sclerotia is currently limited by shortages in pine wood resources. Since protein phosphatases (PPs) play significant roles in growth, signal transduction, development, metabolism, sexual reproduction, cell cycle, and environmental stress responses in fungi, the phosphatome of W. cocos was analyzed in this study by identifying PP genes, studying transcript profiles and assigning PPs to orthologous groups. Fifty-four putative PP genes were putatively identified in W. cocos genome based on homologous sequences searching using BLASTx program against the Saccharomyces cerevisiae, Fusarium graminearum, and Sclerotinia sclerotiorum databases. Based on known and presumed functions of orthologues of these PP genes found in other fungi, the putative roles of these W. cocos PPs in colonization, hyphal growth, sclerotial formation, secondary metabolism, and stress tolerance to environment were discussed in this study. And the level of transcripts from PP genes in the mycelium and sclerotium stages was also analyzed by qRT-PCR. Our study firstly identified and functional discussed the phosphatome in the medicinal and edible fungus W. cocos. The data from our study contribute to a better understanding of PPs potential roles in various cellar processes of W. cocos, and systematically provide comprehensive and novel insights into W. cocos economically important traits that could be extended to other fungi.
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References
Amon A (2008) A decade of Cdc14–a personal perspective delivered on 9 July 2007 at the 32nd FEBS congress in Vienna, Austria. FEBS J 275:5774–5784. doi:10.1111/j.1742-4658.2008.06693.x
Cohen P (2000) The regulation of protein function by multisite phosphorylation–a 25 year update. Trends Biochem Sci 25:596–601. doi:10.1016/S0968-0004(00)01712-6
Dai YC, Yang ZL, Cui BK, Yu CJ, Zhou LW (2009) Species diversity and utilization of medicinal mushrooms and fungi in China. Int J Med Mushrooms 11:287–302. doi:10.1615/IntJMedMushr.v11.i3.80
Doi K, Gartner A, Ammerer G, Errede B, Shinkawa H, Sugimoto K, Matsumoto K (1994) MSG5, a novel protein phosphatase promotes adaptation to pheromone response in Saccharomyces cerevisiae. EMBO J 13:61–70
Du Y, Shi Y, Yang J, Chen X, Xue M, Zhou W, Peng YL (2013) A serine/threonine-protein phosphatase PP2A catalytic subunit is essential for asexual development and plant infection in Magnaporthe oryzae. Curr Genet 59:33–41. doi:10.1007/s00294-012-0385-3
Dubots E, Cottier S, Peli-Gulli MP, Jaquenoud M, Bontron S, Schneiter R, De Virgilio C (2014) TORC1 regulates Pah1 phosphatidate phosphatase activity via the Nem1/Spo7 protein phosphatase complex. PLoS ONE 9:e104194. doi:10.1371/journal.pone.0104194
Erental A, Harel A, Yarden O (2007) Type 2A phosphoprotein phosphatase is required for asexual development and pathogenesis of Sclerotinia sclerotiorum. Mol Plant Microbe Interact 20:944–954. doi:10.1094/MPMI-20-8-0944
Esteban CI (2009) Medicinal interest of Poria cocos (=Wolfiporia extensa). Rev Iberoam Micol 26:103–107. doi:10.1016/S1130-1406(09)70019-1
Feng YL, Lei P, Tian T, Yin L, Chen DQ, Chen H, Mei Q, Zhao YY, Lin RC (2013) Diuretic activity of some fractions of the epidermis of Poria cocos. J Ethnopharmacol 150:1114–1118. doi:10.1016/j.jep.2013.10.043
Gao Y, Yan H, Jin R, Lei P (2016) Antiepileptic activity of total triterpenes isolated from Poria cocos is mediated by suppression of aspartic and glutamic acids in the brain. Pharm Biol 9:1–8. doi:10.3109/13880209.2016.1168853
Gaskell J, Blanchette RA, Stewart PE, BonDurant SS, Adams M, Sabat G, Kersten P, Cullen D (2016) Transcriptome and secretome analyses of the wood decay fungus Wolfiporia cocos support alternative mechanisms of lignocellulose conversion. Appl Environ Microbiol 82:3979–3987. doi:10.1128/AEM.00639-16
Giesbert S, Schumacher J, Kupas V, Espino J, Segmüller N, Haeuser-Hahn I, Schreier P, Tudzynski P (2012) Identification of pathogenesis-associated genes by T-DNA-mediated insertional mutagenesis in Botrytis cinerea: a type 2A phosphoprotein phosphatase and an SPT3 transcription factor have significant impact on virulence. Mol Plant Microbe Interact 25:481–495. doi:10.1094/MPMI-07-11-0199
Harel A, Bercovich S, Yarden O (2006) Calcineurin is required for sclerotial development and pathogenicity of Sclerotinia sclerotiorum in an oxalic acid-independent manner. Mol Plant Microbe Interact 19:682–693. doi:10.1094/MPMI-19-0682
Jiang J, Yun Y, Yang Q, Shim W-B, Wang Z, Ma Z (2011) A type 2C protein phosphatase FgPtc3 is involved in cell wall integrity, lipid metabolism, and virulence in Fusarium graminearum. PLoS ONE 6:e25311. doi:10.1371/journal.pone.0025311
Karanasios E, Han GS, Xu Z, Carman GM, Siniossoglou S (2010) A phosphorylation-regulated amphipathic helix controls the membrane translocation and function of the yeast phosphatidate phosphatase. P Natl Acad Sci USA 107:17539–17544. doi:10.1073/pnas.1007974107
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. doi:10.1007/s11418-011-0612-0
Kubo T, Terabayashi S, Takeda S, Sasaki H, Aburada M, Miyamoto K (2006) Indoor cultivation and cultural characteristics of Wolfiporia cocos sclerotia using mushroom culture bottles. Biol Pharm Bull 29:1191–1196. doi:10.1248/bpb.29.1191
Kumar S, Yoshizumi T, Hongo H, Yoneda A, Hara H, Hamasaki H, Takahashi N, Nagata N, Shimada H, Matsui M (2012) Arabidopsis mitochondrial protein TIM50 affects hypocotyl cell elongation through intracellular ATP level. Plant Sci 183:212–217. doi:10.1016/j.plantsci.2011.08.014
Lee CM, Nantel A, Jiang L, Whiteway M, Shen SH (2004) The serine/threonine protein phosphatase SIT4 modulates yeast-to-hypha morphogenesis and virulence in Candida albicans. Mol Microbiol 51:691–709. doi:10.1111/j.1365-2958.2003.03879.x
Li C, Shi L, Chen D, Ren A, Gao T, Zhao M (2015) Functional analysis of the role of glutathione peroxidase (GPx) in the ROS signaling pathway, hyphal branching and the regulation of ganoderic acid biosynthesis in Ganoderma lucidum. Fungal Genet Biol 82:168–180. doi:10.1016/j.fgb.2015.07.008
Lin ZH, Xiao ZB, Zhu DN, Yan YQ, Yu BY, Wang QJ (2009) Aqueous extracts of FBD, a Chinese herb formula composed of Poria cocos, Atractylodes macrocephala, and Angelica sinensis reverse scopolamine induced memory deficit in ICR mice. Pharm Biol 47:396–401. doi:10.1080/13880200902758816
Miermont A, Uhlendorf J, McClean M, Hersen P (2011) The dynamical systems properties of the HOG signaling cascade. J Signal Transduct 2011:930940. doi:10.1155/2011/930940
Miranda MN, Masuda CA, Ferreira-Pereira A, Carvajal E, Ghislain M, Montero-Lomelí M (2010) The serine/threonine protein phosphatase Sit4p activates multidrug resistance in Saccharomyces cerevisiae. FEMS Yeast Res 10:674–686. doi:10.1111/j.1567-1364.2010.00656.x
Ren A, Liu R, Miao ZG, Zhang X, Cao PF, Chen TX, Li CY, Shi L, Jiang AL, Zhao MW (2017) Hydrogen-rich water regulates effects of ROS balance on morphology, growth and secondary metabolism via glutathione peroxidase in Ganoderma lucidum. Environ Microbiol 19:566–583. doi:10.1111/1462-2920.13498
Rios JL (2011) Chemical constituents and pharmacological properties of Poria cocos. Planta Med 77:681–691. doi:10.1055/s-0030-1270823
Sacco F, Perfetto L, Castagnoli L, Cesareni G (2012) The human phosphatase interactome: an intricate family portrait. FEBS Lett 586:2732–2739. doi:10.1016/j.febslet.2012.05.008
Sakumoto N, Yamashita H, Mukai Y, Kaneko Y, Harashima S (2001) Dual-specificity protein phosphatase Yvh1p, which is required for vegetative growth and sporulation, interacts with yeast pescadillo homolog in Saccharomyces cerevisiae. Biochem Bioph Res C 289:608–615. doi:10.1006/bbrc.2001.6021
Seshacharyulu P, Pandey P, Datta K, Batra SK (2013) Phosphatase: PP2A structural importance, regulation and its aberrant expression in cancer. Cancer Lett 335:9–18. doi:10.1016/j.canlet.2013.02.036
Shi Y (2009) Serine/threonine phosphatases: mechanism through structure. Cell 139:468–484. doi:10.1016/j.cell.2009.10.006
Shu S, Chen B, Zhou M, Zhao X, Xia H, Wang M (2013) De Novo sequencing and transcriptome analysis of Wolfiporia cocos to reveal genes related to biosynthesis of triterpenoids. PLoS ONE 8:e71350. doi:10.1371/journal.pone.0071350
Son S, Osmani SA (2009) Analysis of all protein phosphatase genes in Aspergillus nidulans identifies a new mitotic regulator, fcp1. Eukaryot Cell 8:573–585. doi:10.1128/EC.00346-08
Sun Q, Wei W, Zhao J, Song J, Peng F, Zhang S, Zheng Y, Chen P, Zhu W (2015) An efficient PEG/CaCl2-mediated transformation approach for the medicinal fungus Wolfiporia cocos. J Microbiol Biotechn 25:1528–1531. doi:10.4014/jmb.1501.01053
Tang J, Nie J, Li D, Zhu W, Zhang S, Ma F, Sun Q, Song J, Zheng Y, Chen P (2014) Characterization and antioxidant activities of degraded polysaccharides from Poria cocos sclerotium. Carbohyd Polym 105:121–126. doi:10.1016/j.carbpol.2014.01.049
Wang KQ, Yin XR, Huang H, Fu J, Feng HG, Wang Q, Sun G (2012) Production status and industrialization development countermeasures of Poria in Hubei Province. Modern Chinese Medicine 14:24–27
Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138. doi:10.1093/bioinformatics/btp612
Wang Y, Jiao TL, Liu XH, Lin FC, Wu WR (2011) Functional characterization of a NEM1-like gene in Magnaporthe oryzae. Agr Sci China 10:1385–1390
Wang YZ, Zhang J, Zhao YL, Li T, Shen T, Li JQ, Li WY, Liu HG (2013) Mycology, cultivation, traditional uses, phytochemistry and pharmacology of Wolfiporia cocos (Schwein.) Ryvarden et Gilb.: a review. J Ethnopharmacol 147:265–276. doi:10.1016/j.jep.2013.03.027
Wei W, Shu S, Zhu W, Xiong Y, Peng F (2016) The kinome of edible and medicinal fungus Wolfiporia cocos. Front Microbiol 7:1495. doi:10.3389/fmicb.2016.01495
Wu Y, Zhu W, Wei W, Zhao X, Wang Q, Zeng W, Zheng Y, Chen P, Zhang S (2016) De novo assembly and transcriptome analysis of sclerotial development in Wolfiporia cocos. Gene 588:149–155. doi:10.1016/j.gene.2016.05.020
Xu JW, Xu YN, Zhong JJ (2012) Enhancement of ganoderic acid accumulation by overexpression of an N-terminally truncated 3-hydroxy-3-methylglutaryl coenzyme A reductase gene in the basidiomycete Ganoderma lucidum. Appl Environ Microbiol 78:7968–7976. doi:10.1128/AEM.01263-12
Yang Q, Jiang J, Mayr C, Hahn M, Ma Z (2013) Involvement of two type 2C protein phosphatases BcPtc1 and BcPtc3 in the regulation of multiple stress tolerance and virulence of Botrytis cinerea. Environ Microbiol 15:2696–2711. doi:10.1111/1462-2920.12126
Yu F, Gu Q, Yun Y, Yin Y, Xu JR, Shim WB, Ma Z (2014) The TOR signaling pathway regulates vegetative development and virulence in Fusarium graminearum. New Phytol 203:219–232. doi:10.1111/nph.12776
Yun Y, Liu Z, Yin Y, Jiang J, Chen Y, Xu JR, Ma Z (2015) Functional analysis of the Fusarium graminearum phosphatome. New Phytol 207:119–134. doi:10.1111/nph.13374
Zhang S, Hu B, Wei W, Xiong Y, Zhu W, Peng F, Yu Y, Zheng Y, Chen P (2016) De novo analysis of Wolfiporia cocos transcriptome to reveal the differentially expressed carbohydrate-active enzymes (CAZymes) genes during the early stage of sclerotial growth. Front Microbiol 7:83. doi:10.3389/fmicb.2016.00083
Zhao YY, Feng YL, Bai X, Tan XJ, Lin RC, Mei Q (2013) Ultra performance liquid chromatography-based metabonomic study of therapeutic effect of the surface layer of Poria cocos on adenine-induced chronic kidney disease provides new insight into anti-fibrosis mechanism. PLoS ONE 8:e59617. doi:10.1371/journal.pone.0059617
Zolnierowicz S, Bollen M (2000) Protein phosphorylation and protein phosphatases De Panne, Belgium, September 19–24, 1999. EMBO J 19:483–488. doi:10.1093/emboj/19.4.483
Acknowledgements
We thank the anonymous reviewers for their constructive and helpful comments. This research was supported by Scientific Research Foundation Granted From Wuhan Polytechnic University (2017y12).
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Conceived and designed the experiments: WZ and WW. Performed the experiments: WZ and WW. Analyzed the experiment data: WZ, WW, and SZ. Contributed reagents/materials/analysis tools: WZ, WW, SZ, YZ, and PC. Wrote the paper: WZ and WW. All authors read and approved the final manuscript.
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Zhu, W., Wei, W., Zhang, S. et al. The Phosphatome of Medicinal and Edible Fungus Wolfiporia cocos . Curr Microbiol 75, 124–131 (2018). https://doi.org/10.1007/s00284-017-1356-1
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DOI: https://doi.org/10.1007/s00284-017-1356-1