Abstract
To provide a better understanding of the genetic architecture of fruiting body formation of Lentinula edodes, quantitative trait loci (QTLs) mapping was employed to uncover the loci underlying seven fruiting body-related traits (FBRTs). An improved L. edodes genetic linkage map, comprising 572 markers on 12 linkage groups with a total map length of 983.7 cM, was constructed by integrating 82 genomic sequence-based insertion-deletion (InDel) markers into a previously published map. We then detected a total of 62 QTLs for seven target traits across two segregating testcross populations, with individual QTLs contributing 5.5 %–30.2 % of the phenotypic variation. Fifty-three out of the 62 QTLs were clustered in six QTL hotspots, suggesting the existence of main genomic regions regulating the morphological characteristics of fruiting bodies in L. edodes. A stable QTL hotspot on MLG2, containing QTLs for all investigated traits, was identified in both testcross populations. QTLs for related traits were frequently co-located on the linkage groups, demonstrating the genetic basis for phenotypic correlation of traits. Meta-QTL (mQTL) analysis was performed and identified 16 mQTLs with refined positions and narrow confidence intervals (CIs). Nine genes, including those encoding MAP kinase, blue-light photoreceptor, riboflavin-aldehyde-forming enzyme and cyclopropane-fatty-acyl-phospholipid synthase, and cytochrome P450s, were likely to be candidate genes controlling the shape of fruiting bodies. The study has improved our understanding of the genetic architecture of fruiting body formation in L. edodes. To our knowledge, this is the first genome-wide QTL detection of FBRTs in L. edodes. The improved genetic map, InDel markers and QTL hotspot regions revealed here will assist considerably in the conduct of future genetic and breeding studies of L. edodes.
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References
Akiyama R, Sato Y, Kajiwara S, Shishido K (2002) Cloning and expression of cytochrome P450 genes, belonging to a new P450 family, of the basidiomycete Lentinula edodes. Biosci Biotechnol Biochem 66:2183–2188
Arcade A, Labourdette A, Falque M, Mangin B, Chardon F, Charcosset A, Joets J (2004) BioMercator: integrating genetic maps and QTL towards discovery of candidate genes. Bioinformatics 20:2324–2326
Chen Y, Lübberstedt T (2010) Molecular basis of trait correlations. Trends Plant Sci 15:454–461
Chum WW, Ng KT, Shih RS, Au CH, Kwan HS (2008) Gene expression studies of the dikaryotic mycelium and primordium of Lentinula edodes by serial analysis of gene expression. Mycol Res 112:950–964
Collard BCY, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc Lond Ser B Biol Sci 363:557–572
Costa F (2015) Meta QTL analysis provides a compendium of genomic loci controlling fruit quality traits in apple. Tree Genet Genomes 11:1–11
Foulongne-Oriol M (2012) Genetic linkage mapping in fungi: current state, applications, and future trends. Appl Microbiol Biotechnol 95:891–904
Foulongne-Oriol M, Rodier A, Rousseau T, Savoie JM (2012a) Quantitative trait locus mapping of yield-related components and oligogenic control of the cap color of the button mushroom, Agaricus bisporus. Appl Environ Microbiol 78:2422–2434
Foulongne-Oriol M, Rodier A, Savoie JM (2012b) Relationship between yield components and partial resistance to Lecanicillium fungicola in the button mushroom, Agaricus bisporus, assessed by quantitative trait locus mapping. Appl Environ Microbiol 78:2435–2442
Foulongne-Oriol M, Navarro P, Spataro C, Ferrer N, Savoie JM (2014) Deciphering the ability of Agaricus bisporus var. burnettii to produce mushrooms at high temperature (25 °C). Fungal Genet Biol 73:1–11
Gao W, Weijn A, Baars JJ, Mes JJ, Visser RG, Sonnenberg AS (2015) Quantitative trait locus mapping for bruising sensitivity and cap color of Agaricus bisporus (button mushrooms). Fungal Genet Biol 77:69–81
Goffinet B, Gerber S (2000) Quantitative trait loci: a meta-analysis. Genetics 155:463–473
Gong WB, Liu W, Lu YY, Bian YB, Zhou Y, Kwan HS, Cheung MK, Xiao Y (2014a) Constructing a new integrated genetic linkage map and mapping quantitative trait loci for vegetative mycelium growth rate in Lentinula edodes. Fungal Biol 118:295–308
Gong WB, Xu R, Xiao Y, Zhou Y, Bian YB (2014b) Phenotypic evaluation and analysis of important agronomic traits in the hybrid and natural populations of Lentinula edodes. Sci Hortic 179:271–276
Hirano T, Sato T, Enei H (2004) Isolation of genes specifically expressed in the fruit body of the edible basidiomycete Lentinula edodes. Biosci Biotechnol Biochem 68:468–472
Khowaja FS, Norton GJ, Courtois B, Price AH (2009) Improved resolution in the position of drought-related QTLs in a single mapping population of rice by meta-analysis. BMC Genomics 10:276
Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291
Kosambi DD (1943) The estimation of map distance from recombination values. Ann Eugen 12:172–175
Kwan HS, Au CH, Wong MC, Qin J, Kwok ISW, Chum WWY, Yip PY, Wong KS, Li L, Huang QL, Nong YW (2012) Genome sequence and genetic linkage analysis of Shiitake mushroom Lentinula edodes. Nature Precedings. doi:10.1038/npre.2012.6855.1
Larraya LM, Idareta E, Arana D, Ritter E, Pisabarro AG, Ramírez L (2002) Quantitative trait loci controlling vegetative growth rate in the edible basidiomycete Pleurotus ostreatus. Appl Environ Microbiol 68:1109–1114
Larraya LM, Alfonso M, Pisabarro AG, Ramírez L (2003) Mapping of genomic regions (quantitative trait loci) controlling production and quality in industrial cultures of the edible basidiomycete Pleurotus ostreatus. Appl Environ Microbiol 69:3617–3625
Li H, Durbin R (2009) Fast and accurate short read alignment with burrows–wheeler transform. Bioinformatics 25:1754–1760
Li H, Ye G, Wang J (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175:361–374
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079
Li JZ, Zhang ZW, Li YL, Wang QL, Zhou YG (2011) QTL consistency and meta-analysis for grain yield components in three generations in maize. Theor Appl Genet 122:771–782
Liu Y, Srivilai P, Loos S, Aebi M, Kües U (2006) An essential gene for fruiting body initiation in the basidiomycete Coprinopsis cinerea is homologous to bacterial cyclopropane fatty acid synthase genes. Genetics 172:873–884
Liu G, Jia L, Lu L, Qin D, Zhang J, Guan P, Ni Z, Yao Y, Sun Q, Peng H (2014) Mapping QTLs of yield-related traits using RIL population derived from common wheat and Tibetan semi-wild wheat. Theor Appl Genet 127:2415–2432
Mackay TFC, Stone EA, Ayroles JF (2009) The genetics of quantitative traits: challenges and prospects. Nat Rev Genet 10:565–577
Marathi B, Guleria S, Mohapatra T, Parsad R, Mariappan N, Kurungara VK, Atwal SS, Prabhu KV, Singh NK, Singh AK (2012) QTL analysis of novel genomic regions associated with yield and yield related traits in new plant type based recombinant inbred lines of rice (Oryza sativa L.). BMC Plant Biol 12:137
Miyazaki Y, Nakamura M, Babasaki K (2005) Molecular cloning of developmentally specific genes by representational difference analysis during the fruiting body formation in the basidiomycete Lentinula edodes. Fungal Genet Biol 42:493–505
Miyazaki K, Huang F, Zhang B, Shiraishi S, Sakai M, Shimaya C, Shishido K (2008) Genetic map of a basidiomycete fungus, Lentinula edodes (shiitake mushroom), constructed by tetrad analysis. Breeding Sci 58:23–30
Moquet F, Desmerger C, Mamoun M, Ramos-Guedes-Lafargue M, Olivier JM (1999) A quantitative trait locus of Agaricus bisporus resistance to Pseudomonas tolaasii is closely linked to natural cap color. Fungal Genet Biol 28:34–42
Muraguchi H, Kamada T (2000) A mutation in the eln2 gene encoding a cytochrome P450 of Coprinus cinereus affects mushroom morphogenesis. Fungal Genet Biol 29:49–59
Özçelik E, Pekşen A (2007) Hazelnut husk as a substrate for the cultivation of shiitake mushroom (Lentinula edodes). Bioresour Technol 98:2652–2658
Park J, Lee S, Choi J, Ahn K, Park B, Park J, Kang S, Lee YH (2008) Fungal cytochrome P450 database. BMC Genomics 9:402
Rae AM, Street NR, Robinson KM, Harris N, Taylor G (2009) Five QTL hotspots for yield in short rotation coppice bioenergy poplar: the poplar biomass loci. BMC Plant Biol 9:23
Said JI, Lin Z, Zhang X, Song M, Zhang J (2013) A comprehensive meta QTL analysis for fiber quality, yield, yield related and morphological traits, drought tolerance, and disease resistance in tetraploid cotton. BMC Genomics 14:776
Sano H, Narikiyo T, Kaneko S, Yamazaki T, Shishido K (2007) Sequence analysis and expression of a blue-light photoreceptor gene, Le.phrA from the basidiomycetous mushroom Lentinula edodes. Biosci Biotechnol Biochem 71:2206–2213
Santoyo F, González AE, Terrón MC, Ramírez L, Pisabarro AG (2008) Quantitative linkage mapping of lignin-degrading enzymatic activities in Pleurotus ostreatus. Enzyme Microb Tech 43:137–143
Semagn K, Beyene Y, Warburton ML, Tarekegne A, Mugo S, Meisel B, Sehabiague P, Prasanna BM (2013) Meta-analyses of QTL for grain yield and anthesis silking interval in 18 maize populations evaluated under water-stressed and well-watered environments. BMC Genomics 14:313
Sivolapova AB, Shnyreva AV, Sonnenberg A, Baars I (2012) DNA marking of some quantitative trait loci in the cultivated edible mushroom Pleurotus ostreatus (Fr.) Kumm. Russ J Genet 48:383–389
Sreenivasaprasad S, Eastwood DC, Browning N, Lewis SM, Burton KS (2006) Differential expression of a putative riboflavin-aldehyde-forming enzyme (raf) gene during development and post-harvest storage and in different tissue of the sporophore in Agaricus bisporus. Appl Microbiol Biotechnol 70:470–476
Swamy BM, Vikram P, Dixit S, Ahmed HU, Kumar A (2011) Meta-analysis of grain yield QTL identified during agricultural drought in grasses showed consensus. BMC Genomics, 12:319
Szeto YY, Leung GS, Kwan HS (2007) Le.MAPK and its interacting partner, Le.DRMIP, in fruiting body development in Lentinula edodes. Gene 393:87–93
Tachibana S, Oka M (1981) Occurrence of a vitamin B2-aldehydeforming enzyme in Schizophyllum commune. J Biol Chem 256:6682–6685
Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0 software for the calculation of genetic linkage maps. Plant Research International, Wageningen, The Netherlands
Varshney RK, Thudi M, Nayak SN, Gaur PM, Kashiwagi J, Krishnamurthy L, Jaganathan D, Koppolu J, Bohra A, Tripathi S, Rathore A, Jukanti AK, Jayalakshmi V, Vemula A, Singh SJ, Yasin M, Sheshshayee MS, Viswanatha KP (2014) Genetic dissection of drought tolerance in chickpea (Cicer arietinum L.). Theor Appl Genet 127:445–462
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wang S, Bastern CJ, Zeng ZB (2012) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. (http://statgen.ncsu.edu/qtlcart/WQTLCart.htm)
Zeng Z (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468
Acknowledgments
This work was supported by the National Natural Science Foundation of China (Grant No. 31372117; 31000929), the industry (agriculture), the Science and Technology Plans of Hubei Province (Grant No. 2012DBA19001) and the Fundamental Research Funds for the Central Universities of China (Grant No. 2012ZYTS041).
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Gong, Wb., Li, L., Zhou, Y. et al. Genetic dissection of fruiting body-related traits using quantitative trait loci mapping in Lentinula edodes . Appl Microbiol Biotechnol 100, 5437–5452 (2016). https://doi.org/10.1007/s00253-016-7347-5
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DOI: https://doi.org/10.1007/s00253-016-7347-5