Applied Microbiology and Biotechnology

, Volume 100, Issue 12, pp 5437–5452 | Cite as

Genetic dissection of fruiting body-related traits using quantitative trait loci mapping in Lentinula edodes

  • Wen-bing Gong
  • Lei Li
  • Yan Zhou
  • Yin-bing Bian
  • Hoi-shan Kwan
  • Man-kit Cheung
  • Yang Xiao
Applied genetics and molecular biotechnology

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.

Keywords

Shiitake mushroom Fruiting body-related traits QTL co-localisation QTL hotspots Candidate genes 

Supplementary material

253_2016_7347_MOESM1_ESM.pdf (188 kb)
ESM 1(PDF 188 kb)

References

  1. 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 66:2183–2188CrossRefPubMedGoogle Scholar
  2. 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 20:2324–2326CrossRefPubMedGoogle Scholar
  3. Chen Y, Lübberstedt T (2010) Molecular basis of trait correlations. Trends Plant Sci 15:454–461CrossRefPubMedGoogle Scholar
  4. 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 112:950–964CrossRefPubMedGoogle Scholar
  5. 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 363:557–572CrossRefGoogle Scholar
  6. Costa F (2015) Meta QTL analysis provides a compendium of genomic loci controlling fruit quality traits in apple. Tree Genet Genomes 11:1–11CrossRefGoogle Scholar
  7. Foulongne-Oriol M (2012) Genetic linkage mapping in fungi: current state, applications, and future trends. Appl Microbiol Biotechnol 95:891–904CrossRefPubMedGoogle Scholar
  8. 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 78:2422–2434CrossRefPubMedPubMedCentralGoogle Scholar
  9. 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 78:2435–2442CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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 73:1–11CrossRefPubMedGoogle Scholar
  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 77:69–81CrossRefPubMedGoogle Scholar
  12. Goffinet B, Gerber S (2000) Quantitative trait loci: a meta-analysis. Genetics 155:463–473PubMedPubMedCentralGoogle Scholar
  13. 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 118:295–308CrossRefPubMedGoogle Scholar
  14. 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 179:271–276CrossRefGoogle Scholar
  15. 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 68:468–472CrossRefPubMedGoogle Scholar
  16. 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 10:276CrossRefPubMedPubMedCentralGoogle Scholar
  17. Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291CrossRefPubMedGoogle Scholar
  18. Kosambi DD (1943) The estimation of map distance from recombination values. Ann Eugen 12:172–175CrossRefGoogle Scholar
  19. 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 Google Scholar
  20. 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 68:1109–1114CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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 69:3617–3625CrossRefPubMedPubMedCentralGoogle Scholar
  22. Li H, Durbin R (2009) Fast and accurate short read alignment with burrows–wheeler transform. Bioinformatics 25:1754–1760CrossRefPubMedPubMedCentralGoogle Scholar
  23. Li H, Ye G, Wang J (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175:361–374CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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 25:2078–2079CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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 122:771–782CrossRefPubMedGoogle Scholar
  26. 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 172:873–884CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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 127:2415–2432CrossRefPubMedGoogle Scholar
  28. Mackay TFC, Stone EA, Ayroles JF (2009) The genetics of quantitative traits: challenges and prospects. Nat Rev Genet 10:565–577CrossRefPubMedGoogle Scholar
  29. 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 12:137CrossRefPubMedPubMedCentralGoogle Scholar
  30. 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 42:493–505CrossRefPubMedGoogle Scholar
  31. 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 58:23–30CrossRefGoogle Scholar
  32. 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 28:34–42CrossRefPubMedGoogle Scholar
  33. Muraguchi H, Kamada T (2000) A mutation in the eln2 gene encoding a cytochrome P450 of Coprinus cinereus affects mushroom morphogenesis. Fungal Genet Biol 29:49–59CrossRefPubMedGoogle Scholar
  34. Özçelik E, Pekşen A (2007) Hazelnut husk as a substrate for the cultivation of shiitake mushroom (Lentinula edodes). Bioresour Technol 98:2652–2658CrossRefPubMedGoogle Scholar
  35. Park J, Lee S, Choi J, Ahn K, Park B, Park J, Kang S, Lee YH (2008) Fungal cytochrome P450 database. BMC Genomics 9:402CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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 9:23CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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 14:776CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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 71:2206–2213CrossRefPubMedGoogle Scholar
  39. 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 43:137–143CrossRefGoogle Scholar
  40. 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 14:313CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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 48:383–389CrossRefGoogle Scholar
  42. 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 70:470–476CrossRefPubMedGoogle Scholar
  43. 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, 12:319CrossRefPubMedPubMedCentralGoogle Scholar
  44. Szeto YY, Leung GS, Kwan HS (2007) Le.MAPK and its interacting partner, Le.DRMIP, in fruiting body development in Lentinula edodes. Gene 393:87–93CrossRefPubMedGoogle Scholar
  45. Tachibana S, Oka M (1981) Occurrence of a vitamin B2-aldehydeforming enzyme in Schizophyllum commune. J Biol Chem 256:6682–6685PubMedGoogle Scholar
  46. Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0 software for the calculation of genetic linkage maps. Plant Research International, Wageningen, The NetherlandsGoogle Scholar
  47. 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 127:445–462CrossRefPubMedPubMedCentralGoogle Scholar
  48. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78CrossRefPubMedGoogle Scholar
  49. 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)
  50. Zeng Z (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Wen-bing Gong
    • 1
    • 2
  • Lei Li
    • 3
  • Yan Zhou
    • 1
  • Yin-bing Bian
    • 1
  • Hoi-shan Kwan
    • 3
  • Man-kit Cheung
    • 3
  • Yang Xiao
    • 1
  1. 1.Institute of Applied MycologyHuazhong Agricultural UniversityWuhanPeople’s Republic of China
  2. 2.Institute of Bast Fiber CropsChinese Academy of Agricultural SciencesChangshaPeople’s Republic of China
  3. 3.School of Life SciencesThe Chinese University of Hong KongHong Kong SARPeople’s Republic of China

Personalised recommendations