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http://dx.doi.org/10.1080/12298093.2021.1940746

Evaluation of Genetic Diversity and Population Structure Analysis among Germplasm of Agaricus bisporus by SSR Markers  

An, Hyejin (Department of Industrial Plant Science and Technology, Chungbuk National University)
Lee, Hwa-Yong (Department of Forest Science, Chungbuk National University)
Shin, Hyeran (Department of Industrial Plant Science and Technology, Chungbuk National University)
Bang, Jun Hyoung (Department of Industrial Plant Science and Technology, Chungbuk National University)
Han, Seahee (Department of Industrial Plant Science and Technology, Chungbuk National University)
Oh, Youn-Lee (Department of Herbal Crop Research, National Institute of Horticultural and Herbal Science)
Jang, Kab-Yeul (Department of Herbal Crop Research, National Institute of Horticultural and Herbal Science)
Cho, Hyunwoo (Department of Industrial Plant Science and Technology, Chungbuk National University)
Hyun, Tae Kyung (Department of Industrial Plant Science and Technology, Chungbuk National University)
Sung, Jwakyung (Department of Crop Science, Chungbuk National University)
So, Yoon-Sup (Department of Crop Science, Chungbuk National University)
Jo, Ick-Hyun (Department of Herbal Crop Research, National Institute of Horticultural and Herbal Science)
Chung, Jong-Wook (Department of Industrial Plant Science and Technology, Chungbuk National University)
Publication Information
Mycobiology / v.49, no.4, 2021 , pp. 376-384 More about this Journal
Abstract
Agaricus bisporus is a popular edible mushroom that is cultivated worldwide. Due to its secondary homothallic nature, cultivated A. bisporus strains have low genetic diversity, and breeding novel strains is challenging. The aim of this study was to investigate the genetic diversity and population structure of globally collected A. bisporus strains using simple sequence repeat (SSR) markers. Agaricus bisporus strains were divided based on genetic distance-based groups and model-based subpopulations. The major allele frequency (MAF), number of genotypes (NG), number of alleles (NA), observed heterozygosity (HO), expected heterozygosity (HE), and polymorphic information content (PIC) were calculated, and genetic distance, population structure, genetic differentiation, and Hardy-Weinberg equilibrium (HWE) were assessed. Strains were divided into two groups by distance-based analysis and into three subpopulations by model-based analysis. Strains in subpopulations POP A and POP B were included in Group I, and strains in subpopulation POP C were included in Group II. Genetic differentiation between strains was 99%. Marker AB-gSSR-1057 in Group II and subpopulation POP C was confirmed to be in HWE. These results will enhance A. bisporus breeding programs and support the protection of genetic resources.
Keywords
Agaricus bisporus; genetic diversity; population structure;
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1 Kabel MA, Jurak E, Makela MR, et al. Occurrence and function of enzymes for lignocellulose degradation in commercial Agaricus bisporus cultivation. Appl Microbiol Biotechnol. 2017;101(11): 4363-4369.   DOI
2 Abid G, Mingeot D, Udupa SM, et al. Genetic relationship and diversity analysis of faba bean (Vicia faba L. var. minor) genetic resources using morphological and microsatellite molecular markers. Plant Mol Biol Rep. 2015;33(6): 1755-1767.   DOI
3 Rao VR, Hodgkin T. Genetic diversity and conservation and utilization of plant genetic resources. Plant Cell Tissue Organ Culture. 2002;68(1):1-19.   DOI
4 Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33(7): 1870-1874.   DOI
5 Choudhary G, Ranjitkumar N, Surapaneni M, et al. Molecular genetic diversity of major Indian rice cultivars over decadal periods. PLoS One. 2013;8(6):e66197.   DOI
6 Hamrick JL, Godt MW. Allozyme diversity in plant species. In: Brown AHD, Clegg MT, Kahler AL, Weir BS, editors. Plant population genetics, breeding, and genetic resources. Sunderland: Sinauer Associates Inc.; 1990. p. 43-63.
7 Sonnenberg ASM, Baars JJP, Gao W, et al. Developments in breeding of Agaricus bisporus var. bisporus: progress made and technical and legal hurdles to take. Appl Microbiol Biotechnol. 2017;101(5):1819-1829.   DOI
8 Callac P, Imbernon M, Kerrigan RW, et al. The two life cycles of Agaricus bisporus. In Mushroom biology and mushroom products. University Park, PA: Pennsylvania State University; 1996. p. 57-66.
9 Peakall R, Smouse PE. GENALEX 6: genetic analysis in Excel. Mol Ecol Notes. 2006;6(1):288-295.   DOI
10 Pritchard JK, Wen W, Falush D. Documentation for STRUCTURE software: Version 2; 2003.
11 Paradis E. pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics. 2010;26(3):419-420.   DOI
12 Greenbaum G, Templeton AR, Zarmi Y, et al. Allelic richness following population founding events - a stochastic modeling framework incorporating gene flow and genetic drift. PLOS One. 2014;9(12):e115203.   DOI
13 Sharma M, Kantartzi S, Stewart J. Molecular diversity and polymorphism information content of selected Gossypium hirsutum accessions. Summ Ark Cotton Res. 2009;582:124-126.
14 Nei M, Chesser RK. Estimation of fixation indices and gene diversities. Ann Hum Genet. 1983;47(3): 253-259.   DOI
15 Miah G, Rafii MY, Ismail MR, et al. A review of microsatellite markers and their applications in rice breeding programs to improve blast disease resistance. Int J Mol Sci. 2013;14(11):22499-22528.   DOI
16 Fu Y, Wang X, Li D, et al. Identification of resistance to wet bubble disease and genetic diversity in wild and cultivated strains of Agaricus bisporus. IJMS. 2016;17(10):1568.   DOI
17 Lee H-Y, Moon S, Ro H-S, et al. Analysis of genetic diversity and population structure of wild strains and cultivars using genomic SSR markers in Lentinula edodes. Mycobiology. 2020;48(2): 115-121.   DOI
18 Zhang R, Hu D, Zhang J, et al. Development and characterization of simple sequence repeat (SSR) markers for the mushroom Flammulina velutipes. J Biosci Bioeng. 2010;110(3):273-275.   DOI
19 Moore AJ, Challen MP, Warner PJ, et al. RAPD discrimination of Agaricus bisporus mushroom cultivars. Appl Microbiol Biotechnol. 2001;55(6): 742-749.   DOI
20 Earl DA, vonHoldt BM. Structure harvester: a website and program for visualizing Structure output and implementing the Evanno method. Conservation Genet Resour. 2012;4(2):359-361.   DOI
21 Oh Y-L, Choi I-G, Kong W-S, et al. Evaluating genetic diversity of Agaricus bisporus accessions through phylogenetic analysis using single-nucleotide polymorphism (SNP) markers. Mycobiology. 2020;49(1):61-68.
22 Fu Y-B. Understanding crop genetic diversity under modern plant breeding. Theor Appl Genet. 2015;128(11):2131-2142.   DOI
23 Lee H-Y, Raveendar S, An H, et al. Development of polymorphic simple sequence repeat markers using high-throughput sequencing in button mushroom (Agaricus bisporus). Mycobiology. 2018; 46(4):421-428.   DOI
24 Wang L-n, Gao W, Wang Q-y, et al. Identification of commercial cultivars of Agaricus bisporus in China using genome-wide microsatellite markers. J Integr Agric. 2019;18(3):580-589.   DOI
25 Xu J, Kerrigan RW, Callac P, et al. Genetic structure of natural populations of Agaricus bisporus, the commercial button mushroom. J Heredity. 1997;88(6):482-488.   DOI
26 Kalia RK, Rai MK, Kalia S, et al. Microsatellite markers: an overview of the recent progress in plants. Euphytica. 2011;177(3):309-334.   DOI
27 Foulongne-Oriol M, Spataro C, Savoie J-M. Novel microsatellite markers suitable for genetic studies in the white button mushroom Agaricus bisporus. Appl Microbiol Biotechnol. 2009;84(6):1125-1135.   DOI
28 Malekzadeh K, Shahri BJM, Mohsenifard E. Use of ISSR markers for strain identification in the button mushroom, Agaricus bisporus. In Proceedings of the 7th international conference on mushroom biology and mushroom products (ICMBMP7). 2011. Citeseer.
29 Grunwald NJ, Everhart SE, Knaus BJ, et al. Best practices for population genetic analyses. Phytopathology. 2017;107(9):1000-1010.   DOI
30 Schaid DJ, Batzler AJ, Jenkins GD, et al. Exact tests of Hardy-Weinberg equilibrium and homogeneity of disequilibrium across strata. Am J Hum Genet. 2006;79(6):1071-1080.   DOI
31 Xiang X, Li C, Li L, et al. Genetic diversity and population structure of Chinese Lentinula edodes revealed by InDel and SSR markers. Mycol Prog. 2016;15(4):37.   DOI
32 Sonnenberg A, et al. Breeding and strain protection in the button mushroom Agaricus bisporus. In Proceedings of the 7th International Conference of the World Society for Mushroom Biology and Mushroom Products, 4-7 October 2011, Arcachon, France. 2011.
33 Lee H-Y, Moon S, Shim D, et al. Development of 44 novel polymorphic SSR markers for determination of shiitake mushroom (Lentinula edodes) cultivars. Genes. 2017;8(4):109.   DOI
34 Royse DJ, BJ, Tan Q. Edible and medicinal mushrooms: technology and applications. In: Zied DC, Pardo-Gimenez A, editors. Edible and medicinal mushrooms: technology and applications. New York, NY: John Wiley & Sons Ltd; 2017. p. 5-13.
35 Reis FS, Barros L, Martins A, et al. Chemical composition and nutritional value of the most widely appreciated cultivated mushrooms: an inter-species comparative study. Food Chem Toxicol. 2012; 50(2):191-197.   DOI
36 Chen S, Oh S-R, Phung S, et al. Anti-aromatase activity of phytochemicals in white button mushrooms (Agaricus bisporus). Cancer Res. 2006; 66(24):12026-12034.   DOI
37 Jeong SC, Jeong YT, Yang BK, et al. White button mushroom (Agaricus bisporus) lowers blood glucose and cholesterol levels in diabetic and hypercholesterolemic rats. Nutr Res. 2010;30(1):49-56.   DOI
38 Lopez PA, Widrlechner MP, Simon PW, et al. Assessing phenotypic, biochemical, and molecular diversity in coriander (Coriandrum sativum L.) germplasm. Genet Resour Crop Evol. 2008;55(2): 247-275.   DOI
39 Agarwal M, Shrivastava N, Padh H. Advances in molecular marker techniques and their applications in plant sciences. Plant Cell Rep. 2008;27(4): 617-631.   DOI
40 Rokni N, Goltapeh EM, Shafeinia A, et al. Evaluation of genetic diversity among some commercial cultivars and Iranian wild strains of Agaricus bisporus by microsatellite markers. Botany. 2016;94(1):9-13.   DOI
41 Liu XB, Feng B, Li J, et al. Genetic diversity and breeding history of winter mushroom (Flammulina velutipes) in China uncovered by genomic SSR markers. Gene. 2016;591(1):227-235.   DOI
42 Zhang RY, Hu DD, Gu JG, et al. Development of SSR markers for typing cultivars in the mushroom Auricularia auricula-judae. Mycol Prog. 2012; 11(2):587-592.   DOI
43 Wang Z, Chen M, Cai Z, et al. DNA fingerprinting of genetic diversity of Agaricus bisporus. In Mushroom biology and mushroom products. In Proceedings of the 7th International Conference on Mushroom Biology and Mushroom Products, Arcachon, France, 4-7 October, 2011. Volume 2. Poster session. 2011. France: Institut National de la Recherche Agronomique (INRA).
44 Loftus M, Moore D, Elliott T. DNA polymorphisms in commercial and wild strains of the cultivated mushroom, Agaricus bisporus. Theor Appl Genet. 1988;76(5):712-718.   DOI
45 Khush RS, Becker E, Wach M. DNA amplification polymorphisms of the cultivated mushroom Agaricus bisporus. Appl Environ Microbiol. 1992; 58(9):2971-2977.   DOI
46 An H, Jo I-H, Oh Y-L, et al. Molecular characterization of 170 new gDNA-SSR markers for genetic diversity in button mushroom (Agaricus bisporus). Mycobiology. 2019;47(4):527-532.   DOI
47 Liu XB, Li J, Yang ZL. Genetic diversity and structure of core collection of winter mushroom (Flammulina velutipes) developed by genomic SSR markers. Hereditas. 2018;155(1):3.   DOI
48 Liu K, Muse SV. PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics. 2005;21(9):2128-2129.   DOI
49 Kamvar ZN, Tabima JF, Grunwald NJ. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ. 2014;2:e281.   DOI
50 Xiao Y, Liu W, Dai Y, et al. Using SSR markers to evaluate the genetic diversity of Lentinula edodes' natural germplasm in China. World J Microbiol Biotechnol. 2010;26(3):527-536.   DOI