Mycological Progress

, 15:37 | Cite as

Genetic diversity and population structure of Chinese Lentinula edodes revealed by InDel and SSR markers

  • Xingjie Xiang
  • Chuang Li
  • Lei Li
  • Yingbing Bian
  • Hoi Shan Kwan
  • Wenyan Nong
  • Man Kit Cheung
  • Yang Xiao
Original Article

Abstract

Genetic diversity and population structure of 88 Chinese Lentinula edodes strains belonging to four geographic populations were inferred from 68 Insertion-Deletion (InDel) and two simple sequence repeat (SSR) markers. The overall values of Shannon’s information index and gene diversity were 0.836 and 0.435, respectively, demonstrating a high genetic diversity in Chinese L. edodes strains. Among the four geographic populations, the Central China population displayed a lower genetic diversity. Multiple analyses resolved two unambiguous genetic groups that corresponded to two regions from which the samples were collected—one was a high-altitude region (region 1) and the other was a low-altitude region (region 2). Results from analysis of molecular variance suggested that the majority of genetic variation was contained within populations (74.8 %). Although there was a strong genetic differentiation between populations (FST = 0.252), the variability of ITS sequences from representative strains of the two regions (<3 %) could not support the existence of cryptic species. Pairwise FST values and Nei’s genetic distances showed that there were relatively lower genetic differentiations and genetic distances between populations from the same region. Geographic distribution could play a vital role in the formation of the observed population structure. Mycelium growth rate and precocity of L. edodes strains displayed significant differences between the two regions. Strains from region 2 grew faster and fructified earlier, which could be a result of adaptation to local environmental factors. To the best of our knowledge, this was the first study on the genetic structure and differentiation between populations, as well as the relationship between genetic structure and phenotypic traits in L. edodes.

Keywords

Shiitake mushroom Population genetics InDel markers Mycelium growth rate Precocity 

Supplementary material

11557_2016_1183_MOESM1_ESM.docx (22 kb)
ESM 1(DOCX 22 kb)
11557_2016_1183_MOESM2_ESM.docx (30 kb)
ESM 2(DOCX 29 kb)

References

  1. Bergemann SE, Miller SL (2002) Size, distribution, and persistence of genets in local populations of the late-stage ectomycorrhizal basidiomycete, Russula brevipes. New Phytol 156:313–320CrossRefGoogle Scholar
  2. Bhattramakki D, Dolan M, Hanafey M, Wineland R, Vaske D, Register IJC, Tingey SV, Rafalski A (2002) Insertion-deletion polymorphisms in 3′ regions of maize genes occur frequently and can be used as highly informative genetic markers. Plant Mol Biol 48:539–547CrossRefPubMedGoogle Scholar
  3. Britten RJ, Rowen L, Williams J, Cameron RA (2003) Majority of divergence between closely related DNA samples is due to indels. Proc Natl Acad Sci U S A 100:4661–4665CrossRefPubMedPubMedCentralGoogle Scholar
  4. Brown EM, Mctaggart LR, Zhang SX, Low DE, Stevens DA, Richardson SE (2013) Phylogenetic analysis reveals a cryptic species Blastomyces gilchristii, sp. nov. within the human pathogenic fungus Blastomyces dermatitidis. PLoS ONE 8:e59237CrossRefPubMedPubMedCentralGoogle Scholar
  5. Carriconde F, Gardes M, Jargeat P, Heilmann-Clausen J, Mouhamadou B, Gryta H (2008) Population evidence of cryptic species and geographical structure in the cosmopolitan ectomycorrhizal fungus, Tricholoma scalpturatum. Microb Ecol 56:513–524CrossRefPubMedGoogle Scholar
  6. Chang S (2005) Witnessing the development of the mushroom industry in China. Acta Edulis Fungi 12:3–19Google Scholar
  7. Chiu SW, Ma AM, Lin FC, Moore D (1996) Genetic homogeneity of cultivated strains of shiitake ( Lentinula edodes) used in China as revealed by the polymerase chain reaction. Mycol Res 100:1393–1399CrossRefGoogle Scholar
  8. Cruse M, Telerant R, Gallagher T, Lee T, Taylor JW (2002) Cryptic species in Stachybotrys chartarum. Mycologia 94:814–822CrossRefPubMedGoogle Scholar
  9. Douhan GW, Vincenot L, Gryta H, Selosse MA (2011) Population genetics of ectomycorrhizal fungi: from current knowledge to emerging directions. Fungal Biol-UK 115:569–597CrossRefGoogle Scholar
  10. Duncan DB (1975) t tests and intervals for comparisons suggested by the data. Biometrics 31:339–359CrossRefGoogle Scholar
  11. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  12. Finimundy TC, Dillon AJP, Henriques JAP, Ely MR (2014) A review on general nutritional compounds and pharmacological properties of the Lentinula edodes mushroom. Food Nutr Sci 5:1095–1105CrossRefGoogle Scholar
  13. Foulongne-Oriol M (2012) Genetic linkage mapping in fungi: current state, applications, and future trends. Appl Microbiol Biotechnol 95:891–904CrossRefPubMedGoogle Scholar
  14. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, LondonCrossRefGoogle Scholar
  15. Fu LZ, Zhang HY, Wu XQ, Li HB, Wei HL, Wu QQ, Wang LA (2010) Evaluation of genetic diversity in Lentinula edodes strains using RAPD, ISSR and SRAP markers. World J Microb Biotechnol 26:709–716CrossRefGoogle Scholar
  16. Gaitán-Hernández R, Esqueda M, Gutiérrez A, Sánchez A, Beltrán-García M, Mata G (2006) Bioconversion of agrowastes by Lentinula edodes: the high potential of viticulture residues. Appl Microbiol Biotechnol 71:432–439CrossRefPubMedGoogle Scholar
  17. García-Lor A, Luro F, Navarro L, Ollitrault P (2012) Comparative use of InDel and SSR markers in deciphering the interspecific structure of cultivated citrus genetic diversity: a perspective for genetic association studies. Mol Genet Genomics 287:77–94CrossRefPubMedGoogle Scholar
  18. Given DR (1994) Principles and practice of plant conservation. Chapman & Hall, LondonGoogle Scholar
  19. 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-UK 118:295–308Google Scholar
  20. 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-Amsterdam 179:271–276Google Scholar
  21. Gonzalez D, Cubeta MA, Vilgalys R (2006) Phylogenetic utility of indels within ribosomal DNA and beta-tubulin sequences from fungi in the Rhizoctonia solani species complex. Mol Phylogenet Evol 40:459–70CrossRefPubMedGoogle Scholar
  22. Govindaraju DR (1988) Relationship between dispersal ability and levels of gene flow in plants. Oikos 51:31–35Google Scholar
  23. Hamrick JL, Godt MJW (1990) Allozyme diversity in plant species. In: Brown AHD, Clegg MT, Kahler AL, Weir BS (eds) Plant population genetics, breeding, and genetic resources. Sinauer Associates Inc, Sunderland, pp 43–63Google Scholar
  24. Hamrick JL, Godt MJW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. New Forest 6:95–124CrossRefGoogle Scholar
  25. Hartl DL, Clark AG (1997) Principles of population genetics. Sinauer Associates Inc., SunderlandGoogle Scholar
  26. Heinzelmann R, Rigling D, Prospero S (2012) Population genetics of the wood-rotting basidiomycete Armillaria cepistipes in a fragmented forest landscape. Fungal Biol-UK 116:985–994CrossRefGoogle Scholar
  27. Hibbett DS, Hansen K, Donoghue MJ (1998) Phylogeny and biogeography of Lentinula inferred from an expanded rDNA dataset. Mycol Res 102:1041–1049CrossRefGoogle Scholar
  28. James TY, Vilgalys R (2001) Abundance and diversity of Schizophyllum commune spore clouds in the Caribbean detected by selective sampling. Mol Ecol 10:471–479CrossRefPubMedGoogle Scholar
  29. James TY, Porter D, Hamrick JL, Vilgalys R (1999) Evidence for limited intercontinental gene flow in the cosmopolitan mushroom, Schizophyllum commune. Evolution 53:1665–1677CrossRefGoogle Scholar
  30. Kauserud H, Stensrud Ø, Decock C, Shalchian-Tabrizi K, Schumacher T (2006) Multiple gene genealogies and AFLPs suggest cryptic speciation and long-distance dispersal in the basidiomycete Serpula himantioides (Boletales). Mol Ecol 15:421–431CrossRefPubMedGoogle Scholar
  31. Kim KH, Kim YY, Ka KH, Lee HS, Bak WC, Jeong SJ, Seong JY, Suh DS (2009) Microsatellite markers for population-genetic studies of shiitake (Lentinula edodes) strains. Genes Genom 31:403–411CrossRefGoogle Scholar
  32. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedGoogle Scholar
  33. Kwan HS, Au CH, Wong MC, Qin J, Kwok ISW, Chum, WWY, Yip PY, Wong KS, Li L, Huang Q (2012) Genome sequence and genetic linkage analysis of Shiitake mushroom Lentinula edodes. Nature Precedings. doi: 10.1038/npre.2012.6855.1
  34. 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 Microb (AEM) 68:1109–1114CrossRefGoogle Scholar
  35. Larraya LM, Mikel A, Pisabarro AG, Lucía R (2003) Mapping of genomic regions (quantitative trait loci) controlling production and quality in industrial cultures of the edible basidiomycete Pleurotus ostreatus. Appl Environ Microb (AEM) 69:3617–3625CrossRefGoogle Scholar
  36. Li AZ, Xu XF, Lin FX, Cheng SM, Lin FC (2007) Cloning and identification of partial DNA fragment for the B mating-type factor in Lentinula edodes using degenerate PCR. World J Microb Biotechnol 23:411–415CrossRefGoogle Scholar
  37. Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129CrossRefPubMedGoogle Scholar
  38. Liu J, Zheng X, Potter D, Hu C, Teng Y (2012a) Genetic diversity and population structure of Pyrus calleryana (Rosaceae) in Zhejiang province, China. Biochem Syst Ecol 45:69–78Google Scholar
  39. Liu JY, Ying ZH, Fang L, Liu XR, Xie BG (2012b) Evaluation of the use of SCAR markers for screening genetic diversity of Lentinula edodes strains. Curr Microbiol 64:317–25Google Scholar
  40. Liu B, Wang Y, Zhai W, Deng J, Wang H, Cui Y, Cheng F, Wang X, Wu J (2013) Development of InDel markers for Brassica rapa based on whole-genome re-sequencing. Theor Appl Genet (TAG) 126:231–239CrossRefGoogle Scholar
  41. Muller LAH, Vangronsveld J, Colpaert JV (2007) Genetic structure of Suillus luteus populations in heavy metal polluted and nonpolluted habitats. Mol Ecol 16:4728–4737CrossRefPubMedGoogle Scholar
  42. Murray M, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326CrossRefPubMedPubMedCentralGoogle Scholar
  43. Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH (2008) Intraspecific ITS variability in the kingdom Fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol Bioinform 4:193Google Scholar
  44. Ollitrault F, Terol J, Martin AA, Pina JA, Navarro L, Talon M, Ollitrault P (2012) Development of InDel markers from Citrus clementina (Rutaceae) BAC-end sequences and interspecific transferability in Citrus. Am J Bot 99:e268–e273CrossRefPubMedGoogle Scholar
  45. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  46. Philippoussis A, Diamantopoulou P, Israilides C (2007) Productivity of agricultural residues used for the cultivation of the medicinal fungus Lentinula edodes. Int Biodeter Biodegr 59:216–219CrossRefGoogle Scholar
  47. Pritchard JK, Wen X, Falushb D (2009) Documentation for structure software: Version 2.3Google Scholar
  48. Ravash R, Shiran B, Alavi AA, Bayat F, Rajaee S, Zervakis GI (2010) Genetic variability and molecular phylogeny of Pleurotus eryngii species-complex isolates from Iran, and notes on the systematics of Asiatic populations. Mycol Prog 9:181–194CrossRefGoogle Scholar
  49. Rohlf FJ (2000) NTSYS-pc: numerical taxonomy and multivariate analysis system. Version 2.1. Exeter Publications, New YorkGoogle Scholar
  50. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  51. Royse DJ, Sanchez-Vazquez JE (2001) Influence of substrate wood-chip particle size on shiitake ( Lentinula edodes) yield. Bioresour Technol 76:229–233CrossRefPubMedGoogle Scholar
  52. Sadfi-Zouaoui N, Hannachi I, Rouaissi M, Hajlaoui MR, Rubio MB, Monte E, Boudabous A, Hermosa MR (2009) Biodiversity of Trichoderma strains in Tunisia. Can J Microbiol 55:154–162CrossRefPubMedGoogle Scholar
  53. Salmones D, Gaitán-Hernández R, Pérez R, Guzmán G (1997) Studies on genus Pleurotus. VIII. Interaction between mycelial growth and yield. Rev Iberoam Micol 14:173–176PubMedGoogle Scholar
  54. Sica M, Gaudio L, Aceto S (2007) Genetic structure of Tuber mesentericum Vitt. based on polymorphisms at the ribosomal DNA ITS. Mycorrhiza 17:405–414CrossRefPubMedGoogle Scholar
  55. 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
  56. Sun Y, Lin FC (2003) Analysis of genetic diversity in natural germplasm of Lentinula edodes in China using RAPD technique. Mycosystema 22:387–393, in ChineseGoogle Scholar
  57. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  58. Urbanelli S, Della RV, Fanelli C, Fabbri AA, Reverberi M (2003) Genetic diversity and population structure of the Italian fungi belonging to the taxa Pleurotus eryngii (DC.:Fr.) Quèl and P. ferulae (DC.:Fr.) Quèl. Heredity 90:253–2599CrossRefPubMedGoogle Scholar
  59. Väli Ü, Brandström M, Johansson M, Ellegren H (2008) Insertion-deletion polymorphisms (indels) as genetic markers in natural populations. BMC Genet 9:8CrossRefPubMedPubMedCentralGoogle Scholar
  60. van der Nest MA, Slippers B, Steenkamp ET, De Vos L, Van Zyl K, Stenlid J, Wingfield MJ, Wingfield BD (2009) Genetic linkage map for Amylostereum areolatum reveals an association between vegetative growth and sexual and self-recognition. Fungal Genet Biol 46:632–641CrossRefPubMedGoogle Scholar
  61. Vincenot L, Nara K, Sthultz C, Labbe J, Dubois MP, Tedersoo L, Martin F, Selosse MA (2012) Extensive gene flow over Europe and possible speciation over Eurasia in the ectomycorrhizal basidiomycete Laccaria amethystina complex. Mol Ecol 21:281–299CrossRefPubMedGoogle Scholar
  62. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar
  63. Wu K, Yang M, Liu H, Tao Y, Mei J, Zhao Y (2014) Genetic analysis and molecular characterization of Chinese sesame (Sesamum indicum L.) cultivars using Insertion-Deletion (InDel) and Simple Sequence Repeat (SSR) markers. BMC Genet 15:35CrossRefPubMedPubMedCentralGoogle Scholar
  64. Xiao Y, Liu W, Dai YH, Fu C, Bian YB (2010a) Using SSR markers to evaluate the genetic diversity of Lentinula edodes’ natural germplasm in China. World J Microb Biotechnol 26:527–536Google Scholar
  65. Xiao Y, Liu W, Lu YY, Gong WB, Bian YB (2010b) Applying target region amplification polymorphism markers for analyzing genetic diversity of Lentinula edodes in China. J Basic Microb 50:475–483Google Scholar
  66. Xu XF, Li AZ, Chen SM, Lin FC, Lin FX (2005) Genetic diversity of natural germplam of Leninula edodes in China inferred from rDNA sequences. Mycosystema 24:29–35, in ChineseGoogle Scholar
  67. Xu XF, Li AZ, Cheng SM, Lin FX, Lin FC (2006) Reappraisal of phylogenetic status and genetic diversity analysis of Asian population of Lentinula edodes. Prog Nat Sci 16:274–280CrossRefGoogle Scholar
  68. Xu J, Sha T, Li YC, Zhao ZW, Yang ZL (2008) Recombination and genetic differentiation among natural populations of the ectomycorrhizal mushroom Tricholoma matsutake from southwestern China. Mol Ecol 17:1238–1247CrossRefPubMedGoogle Scholar
  69. Yeh F (1997) Population genetic analysis of codominant and dominant markers and quantitative traits. Belg J Bot 129:157Google Scholar
  70. Zhao M, Huang C, Chen Q, Wu X, Qu J, Zhang J (2013) Genetic variability and population structure of the mushroom Pleurotus eryngii var. tuoliensis. PLoS ONE 8:e83253CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© German Mycological Society and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Xingjie Xiang
    • 1
    • 2
  • Chuang Li
    • 1
    • 2
  • Lei Li
    • 3
  • Yingbing Bian
    • 1
    • 2
  • Hoi Shan Kwan
    • 3
  • Wenyan Nong
    • 3
  • Man Kit Cheung
    • 3
  • Yang Xiao
    • 1
    • 2
  1. 1.Key Laboratory of Agro-Microbial Resource and Development (Ministry of Agriculture)Huazhong Agricultural UniversityHubei ProvincePeople’s Republic of China
  2. 2.Institute of Applied MycologyHuazhong Agricultural UniversityHubei ProvincePeople’s Republic of China
  3. 3.School of Life SciencesThe Chinese University of Hong KongHong Kong SARPeople’s Republic of China

Personalised recommendations