Transcriptome analysis and its application in identifying genes associated with fruiting body development in basidiomycete Hypsizygus marmoreus

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Zhang, Jinjing ^a,b,c   Ren, Ang ^a   Chen, Hui ^b,c   Zhao, Mingwen ^a   Shi, Liang ^a   Chen, Mingjie ^b,c   Wang, Hong ^b,c   Feng, Zhiyong ^a,b,c  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

^c INSTITUTE OF EDIBLE FUNGI   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; MITOGEN ACTIVATED PROTEIN KINASE; NITROGEN; TRANSCRIPTOME; CRYPTOCHROME; FUNGAL DNA; REACTIVE OXYGEN METABOLITE; TARGET OF RAPAMYCIN KINASE;

ARTICLE; BASIDIOMYCETES; CONTROLLED STUDY; DATA BASE; DEVELOPMENTAL STAGE; EUKARYOTIC ORTHOLOGOUS GROUP DATABASE; FRUITING BODY; GENE EXPRESSION; GENE ONTOLOGY; GENETIC IDENTIFICATION; HYPSIZYGUS MARMOREUS; KYOTO ENCYCLOPEDIA OF GENE AND GENOME DATABASE; MORPHOGENESIS; MUSHROOM; MYCELIAL GROWTH; NITROGEN METABOLISM; NONHUMAN; PRIMORDIUM; RNA SEQUENCE; SIGNAL TRANSDUCTION; AGARICALES; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MYCELIUM; NUCLEOTIDE SEQUENCE; PIGMENTATION;

BASIDIOMYCOTA; EUKARYOTA; HYPSIZYGUS MARMOREUS;

AGARICALES; BASE SEQUENCE; CRYPTOCHROMES; CYCLIC AMP; DNA, FUNGAL; FRUITING BODIES, FUNGAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; MYCELIUM; NITROGEN; PIGMENTATION; REACTIVE OXYGEN SPECIES; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84926433416     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0123025     Document Type: Article

References (62)

1. Kües U. Life history and development processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Res. 2000; 604: 316-353.
2. Kües U, Liu Y. Fruiting body production in basidiomycetes. Appl Microbiol Biotechnol. 2000; 54: 141-152. PMID: 10968625
3. Wessels JGH. Tansley Review No. 45 Wall growth, protein excretion and morphogenesis in fungi. New Phytol. 1993; 123: 397-413.
4. De Groot PWJ, Visser J, Van Griensven LJLD, Schaap PJ. Biochemical and molecular aspects of growth and fruiting of the edible mushroom Agaricus bisporus. Mycol Res.1998; 102: 1297-1308.
5. Umer MH, Van Griensven LJLD. The role of morphogenetic cell death in histogenesis of the mycelial cord of Agaricus bisporus and in the development of macrofungi. Mycol Res. 1998; 102: 719-735.
6. Mu DS, Li CY, Zhang XC, Shi L, Ren A, Zhao MW. Functions of the nicotinamide adenine dinucleotide phosphate oxidase family in Ganoderma lucidum: an essential role in hyphal branching, fruiting body development, oxidative-stress resistance, and ganoderic acid biosynthesis regulation. Environ Microbioldoi. 2014; 16: 1709-1728. doi: 10.1111/1462-2920.12326 PMID: 24238263
7. Terashima K, Yuki K, Muraguchi H, Akiyama M, Kamada T. The dst1 gene involved in mushroom photomorphogenesis of Coprinus cinereus encodes a putative photoreceptor for blue light. Genetics. 2005; 171: 101-108. PMID: 15956671
8. Kuratani M, Tanaka K, Terashima K, Muraguchi H, Nakazawa T, Kamada T. The dst2 gene essential for photomorphogenesis of Coprinopsis cinerea encodes a protein with a putative FAD-binding-4 domain. Fungal Genet Biol. 2010; 47: 152-158. doi: 10.1016/j.fgb.2009.10.006 PMID: 19850145
9. Nakazawa T, Kondo H, Nakahori K, Kamada T. A mutation in the Cc.ubc2 gene affects clamp cell morphogenesis as well as nuclear migration fordiakaryosis in Coprinopsis cinerea. Fungal Genet Biol. 2011; 48: 519-525. doi: 10.1016/j.fgb.2011.01.010 PMID: 21281729
10. Muraguchi H, Kamada T. A Mutation in the eln2 Gene Encoding a Cytochrome P450 of Coprinus cinereus Affects Mushroom Morphogenesis. Fungal Genet Biol. 2000; 29: 49-59. PMID: 10779399
11. Hsu HK, Lee YR, Lin YL, Chu FH. Cytochrome P450 Genes in Medicinal Mushroom Antrodia cinnamomea T.T. Chang et W.N. Chou (Higher Basidiomycetes) are Strongly Expressed During Fruiting Body Formation. Int J Med Mushrooms. 2011; 13: 513-523. PMID: 22181839
12. Idnurm A, Heitman J. Light Controls Growth and Development via a Conserved Pathway in the Fungal Kingdom. PLoS Biology. 2005; 3: 615-626.
13. Etxebeste O, Herrero-García E, Araújo-Bazán L, Rodríguez-Urra AB, Garzia A, Ugalde U, et al. The bZIP-type transcription factor FlbB regulates distinct morphogenetic stages of colony formation in Aspergillus nidulans. Mol Microbiol. 2009; 73: 775-789. doi: 10.1111/j.1365-2958.2009.06804.x PMID: 19656299
14. Masloff S, Pöggeler S, Kück U. The pro1(+) gene from Sordaria macrospora encodes a C-6 zinc finger transcription factor required for fruiting body development. Genetics. 1999; 152: 191-199. PMID: 10224253
15. Park G, Pan S, Borkovich KA. Mitogen-activated protein kinase cascade required for regulation of development and secondary metabolism in Neurospora crassa. Eukaryot Cell. 2008; 7: 2113-2122. doi: 10.1128/EC.00466-07 PMID: 18849472
16. Palmer GE, Horton JS. Mushrooms by magic: making connections between signal transduction and fruiting body development in the basidiomycete fungus Schizophyllum commune. FEMS Microbiol Lett. 2006; 262: 1-8. PMID: 16907732
17. Lengeler KB, Davidson RC, D'souza C, Harashima T, Shen WC, Wang P, et al. Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev. 2000; 64: 746-785. PMID: 11104818
18. Akavia E, Wasser SP, Beharav A, Nevo E. Study of Hypsizygus marmoreus(Peck) Bigel. And Grifola frondosa (Dicks.: Fr.) S.F. Gray: Cultural-Morphological Peculiarities, Growth Characteristics, Qualitative Enzymatic Activity, and Resistance to Fungal Pest Contamination. Inter J Med Mushrooms. 2006; 8: 361-376.
19. Jang MJ, Lee YH, Ju YC, Kim SM, Koo HM. Effect of Color of Light Emitting Diode on Development of Fruit Body in Hypsizygus marmoreus. Mycobiology. 2013; 41: 63-66. doi: 10.5941/MYCO.2013.41.1. 63 PMID: 23610542
20. Lee CY, Park JE, Lee J, Kim JK, Ro HS. Development of new strains and related SCAR markers for an edible mushroom, Hypsizygus marmoreus. FEMS Microbiol Lett. 2012; 327: 54-59. doi: 10.1111/j. 1574-6968.2011.02458.x PMID: 22093038
21. Zhang JJ, Shi L, Chen H, Sun YQ, Zhao MW, Ren A, et al. An efficient Agrobacterium-mediated transformation method for the edible mushroom Hypsizygus marmoreus. Microbiol Res. 2014; 169: 741-749. doi: 10.1016/j.micres.2014.01.004 PMID: 24612605
22. Cheng CK, Au CH, Wilke SK, Stajich JE, Zolan ME, Pukkila PJ, et al. 5'-Serial Analysis of Gene Expression studies reveal a transcriptomic switch during fruiting body development in Coprinopsis cinerea. BMC Genomics. 2013; 14:195. doi: 10.1186/1471-2164-14-195 PMID: 23514374
23. Yu GJ, Wang M, Huang J, Yin YL, Chen YJ, Jang S, et al. Deep Insight into the Ganoderma lucidum by Comprehensive Analysis of Its Transcriptome. PLoS One. 2012; 7: e44031. doi: 10.1371/journal.pone. 0044031 PMID: 22952861
24. Eastwood DC, Herman B, Noble R, Dobrovin-Pennington A, Sreenivasaprasad S, et al. Environmental regulation of reproductive phase change in Agaricus bisporus by 1-octen-3-ol, temperature and CO2. Fungal Genet Biol. 2013; 55: 54-66. doi: 10.1016/j.fgb.2013.01.001 PMID: 23354075
25. Li P, Deng WQ, Li TH, Song B, Shen YH. Illumina-based de novo transcriptome sequencing and analysis of Amanita exitialis basidiocarps. Gene. 2013; 532: 63-71. doi: 10.1016/j.gene.2013.09.014 PMID: 24050899
26. Wang M, Gu BL, Huang J, Jiang S, Chen YJ, Yin YL, et al. Transcriptome and Proteome Exploration to Provide a Resource for the Study of Agrocybe aegerita. PLoS One. 2013; 8: 1-20.
27. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29: 644-652. doi: 10. 1038/nbt.1883 PMID: 21572440
28. von Mering C, Huynen M, Jaeggi D, Schmidt S, Bork P, Snel B. STRING: a database of predicted functional associations between proteins. Nucleic Acids Res. 2003; 31: 258-261. PMID: 12519996
29. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005; 21: 3674-3676. PMID: 16081474
30. Kanehisa M, Goto S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 2000; 28: 27-30. PMID: 10592173
31. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12: 323. doi: 10.1186/1471-2105-12-323 PMID: 21816040
32. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010; 26: 139-140. doi: 10.1093/ bioinformatics/btp616 PMID: 19910308
33. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008; 5: 621-628. doi: 10.1038/nmeth.1226 PMID: 18516045
34. Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, et al. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 2011; 39: 16-22.
35. Stamets P. Growing gourmet and medicinal mushrooms: [Shokuyo oyobiyakuyo kinoko no saibai]: a companion guide to The mushroom cultivator. Ten Speed Press (Berkeley, CA). 1993; 103: 242-569.
36. Lee YL, Jian SY, Mau JL. Composition and non-volatile taste components of Hypsizigus marmoreus. Food Sci and Tech. 2009; 42: 594-598.
37. Wang LG, Wang SQ, Li W. RSeQC: quality control of RNA-seq experiments. BIOINFORMATICS. 2012; 28: 2184-2185. doi: 10.1093/bioinformatics/bts356 PMID: 22743226
38. Yonekura-Sakakibara K, Tohge T, Matsuda F, Nakabayashi R, Takayama H, Niida R, et al. Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. Plant Cell. 2008; 20: 2160-2176. doi: 10.1105/tpc.108.058040 PMID: 18757557
39. Park HY, Gilchrest BA. Signaling pathways mediating melanogenesis. Cell Mol Biol (Noisy-le-grand). 1999; 45: 919-930. PMID: 10643996
40. Akavia E, Wasser SP, Beharav A, Nevo E. Study of Hypsizygus marmoreus(Peck) Bigel and Grifola frondosa (Dicks.: Fr.) S.F. Gray: Cultural-Morphological Peculiarities, Growth Characteristics, Qualitative Enzymatic Activity, and Resistance to Fungal Pest Contamination. Inter J Med Mushrooms. 2006; 8: 361-376.
41. Jang MJ, Lee YH, Ju YC, Kim SM, Koo HM. Effect of Color of Light Emitting Diode on Development of Fruit Body in Hypsizygus marmoreus. Mycobiology. 2013; 41: 63-66. doi: 10.5941/MYCO.2013.41.1. 63 PMID: 23610542
42. Aleksandrova EA, Zavyalova LA, Tereshina VM, Garibova LV, Feofilova EP. Obtaining of fruiting bodies and submerged mycelium of Lentinus edodes(Berk.) Sing [Lentinula edodes (Berk.) Pegler]. Microbiology. 1998; 67: 535-539.
43. Chum WWY, Ng KTP, Shih RSM, Au CH, Kwan HS. Gene expression studies of the dikaryotic mycelium and primordium of Lentinula edodes by serial analysis of gene expression. Mycol Res. 2008; 112: 950-964. doi: 10.1016/j.mycres.2008.01.028 PMID: 18555678
44. Sano H, Narikiyo T, Kaneko S, Yamazaki T, Shishido K. Sequence analysis and expression of a bluelight photoreceptor gene, Le.phrA from the basidiomycetous mushroom Lentinula edodes. Biosci Biotech Biochem. 2007; 71: 2206-2213. PMID: 17827679
45. Sano H, Kaneko S, Sakamoto Y, Sato T, Shishido K. The basidiomycetous mushroom Lentinula edodes white collar-2 homolog PHRB, a partner of putative blue-light photoreceptor PHRA, binds to a specific site in the promoter region of the L. edodes tyrosinase gene. Fungal Genet Biol. 2009; 46: 333-341. doi: 10.1016/j.fgb.2009.01.001 PMID: 19344689
46. Tang LH, Jian HH, Song CY, Bao DP, Shang XD, Wu DQ, et al. Transcriptome analysis of candidate genes and signaling pathways associated with light-induced brown film formation in Lentinula edodes. Appl Microbiol Biotechnol. 2013; 97: 4977-989. doi: 10.1007/s00253-013-4832-y PMID: 23624682
47. Sanchez-Ferrer A, Rodriguez-Lopez JN, Garcia-Canovas F, Garcia-Carmona F. Tyrosinase: A comprehensive review of its mechanism. Biochim Biophys Acta. 1995; 1247: 1-11. PMID: 7873577
48. Weijn A, Bastiaan-Net S, Wichers HJ, Mes JJ. Melanin biosynthesis pathway in Agaricus bisporus mushrooms. Fungal Genet Biol. 2013; 55: 42-53. doi: 10.1016/j.fgb.2012.10.004 PMID: 23123422
49. Leatham GF, Stahmann MA. Effect of light and aeration on fruiting of Lentinula edodes. Trans Br Mycol Soc. 1987; 88: 9-20.
50. Xu JR. MAP Kinases in Fungal Pathogens. Fungal Genet Biol. 2000; 31: 137-152. PMID: 11273677
51. Katherine PD, Xu JR, Smirnoff N, Talbot NJ. Independent Signaling Pathways Regulate Cellular Turgor during Hyperosmotic Stress and Appressorium-Mediated Plant Infection by Magnaporthegrisea. The Plant Cell. 2000; 11: 2045-2058.
52. Kües U, Kunzler M, Bottoli APF, Walser PJ, Granado JD. Mushroom development in higher basidiomycetes; implications for human and animal health. In:Kushwaha RKS editor. In Fungi in Human and Animal Health. India: Scientific Publishers Rks. 2004. pp. 431-470.
53. Lalucque H, Silar P. NADPH oxidase: an enzyme for multicellularity? Trends Microbiol. 2003; 11: 9-12. PMID: 12526848
54. Takemoto D, Tanaka A, Scott B. Ap67Phox-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis. Plant Cell. 2006; 18: 2807-2821. PMID: 17041146
55. Lara-Ortiz T, Riveros-Rosas H, Aguirre J. Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol Microbiol. 2003; 50: 1241-1255. PMID: 14622412
56. Malagnac F, Lalucque H, Lepere G, Silar P. Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podosporaanserina. Fungal Genet Biol. 2004; 41: 982-997. PMID: 15465387
57. Cano-Dominguez N, Alvarez-Delfin K, HansbergW, Aguirre J. NADPH oxidases NOX-1 and NOX-2 require the regulatory subunit NOR-1 to control cell differentiation and growth in Neurospora crassa. Eukaryot Cell. 2008; 7: 1352-1361. doi: 10.1128/EC.00137-08 PMID: 18567788
58. Lengeler KB, Davidson RC, Dsouza C, Harashima T, Shen WC, Wang P, et al. Signal Transduction Cascades Regulating Fungal Development and Virulence. Microbiol Mol Biol Rev. 2000; 64: 746-785. PMID: 11104818
59. Lilleskov EA, Fahey TJ, Horton TR, Lovett GM. Below ground ectomycorrhizal fungal conmmunity change over a nitrogen deposition gradient in alaska. Ecology. 2002; 83: 104-115.
60. Bidartondo MI, Wallander HEH, Söderström B. Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi? New Phytol. 2001; 151: 543-550.
61. Krieg RC, Dong Y, Schwamborn K, Knuechel R. Protein quantification and its tolerance for different interfering reagents using the BCA-method with regard to 2D SDS PAGE. J Biochem Biophmeth. 2005; 65: 13-19. PMID: 16226314
62. Zhang H, Wang ZY, Yang X, Zhao HT, Zhang YC, Dong AJ, et al. Determination of free amino acids and 18 elements in freeze-dried strawberry and blueberry fruit using an Amino Acid Analyzer and ICPMS with micro-wave digestion. Food Chem. 2014; 147: 189-194. doi: 10.1016/j.foodchem.2013.09. 118 PMID: 24206704