DOI QR코드

DOI QR Code

Determination and Analysis of Hyper-Variable A Mating Types in Wild Strains of Lentinula edodes in Korea

  • Mi-Jeong Park (Forest Microbiology Division, Department of Forest Bio-Resources, National Institute of Forest Science) ;
  • Eunjin Kim (Forest Microbiology Division, Department of Forest Bio-Resources, National Institute of Forest Science) ;
  • Yeun Sug Jeong (Forest Microbiology Division, Department of Forest Bio-Resources, National Institute of Forest Science) ;
  • Mi-Young Son (Forest Microbiology Division, Department of Forest Bio-Resources, National Institute of Forest Science) ;
  • Yeongseon Jang (Forest Microbiology Division, Department of Forest Bio-Resources, National Institute of Forest Science) ;
  • Kang-Hyeon Ka (Forest Microbiology Division, Department of Forest Bio-Resources, National Institute of Forest Science)
  • Received : 2022.11.07
  • Accepted : 2022.12.19
  • Published : 2023.02.28

Abstract

The diversity of A mating type in wild strains of Lentinula edodes was extensively analyzed to characterize and utilize them for developing new cultivars. One hundred twenty-three A mating type alleles, including 67 newly discovered alleles, were identified from 106 wild strains collected for the past four decades in Korea. Based on previous studies and current findings, a total of 130 A mating type alleles have been found, 124 of which were discovered from wild strains, indicating the hyper-variability of A mating type alleles of L. edodes. About half of the A mating type alleles in wild strains were found in more than two strains, whereas the other half of the alleles were found in only one strain. About 90% of A mating type combinations in dikaryotic wild strains showed a single occurrence. Geographically, diverse A mating type alleles were intensively located in the central region of the Korean peninsula, whereas only allele A17 was observed throughout Korea. We also found the conservation of the TCCCAC motif in addition to the previously reported motifs, including ATTGT, ACAAT, and GCGGAG, in the intergenic regions of A mating loci. Sequence comparison among some alleles indicated that accumulated mutation and recombination would contribute to the diversification of A mating type alleles in L. edodes. Our data support the rapid evolution of A mating locus in L. edodes, and would help to understand the characteristics of A mating loci of wild strains in Korea and help to utilize them for developing new cultivars.

Keywords

Acknowledgement

The authors sincerely appreciate Prof. Hyeon-Su Ro and Dr. Sinil Kim at Gyeongsang National University for providing critical advice on the sequence analysis. The authors also thank Sang-Woo Lee for assisting with PCR amplifications and Sujung Yoo for helping to map the collection sites using QGIS.

References

  1. Casselton LA. Mate recognition in fungi. Heredity (Edinb). 2002;88(2):142-147. https://doi.org/10.1038/sj.hdy.6800035
  2. Ni M, Feretzaki M, Sun S, et al. Sex in fungi. Annu Rev Genet. 2011;45:405-430. https://doi.org/10.1146/annurev-genet-110410-132536
  3. Nieuwenhuis BPS, Billiard S, Vuilleumier S, et al. Evolution of uni- and bifactorial sexual compatibility systems in fungi. Heredity (Edinb). 2013;111(6):445-455. https://doi.org/10.1038/hdy.2013.67
  4. Royse DJ, Baars J, Tan Q. Current overview of mushroom production in the world. In: Zied DC, Pardo-Gim enez A, editors. Edible and medicinal mushrooms: technology and applications. Hoboken: John Wiley & Sons Ltd; 2017. p. 5-13.
  5. Bak WC, Park JH, Park YA, et al. Determination of glucan contents in the fruiting bodies and mycelia of Lentinula edodes cultivars. Mycobiology. 2014;42(3):301-304. https://doi.org/10.5941/MYCO.2014.42.3.301
  6. Gait an-Hernandez R, Lopez-Pena D, Esqueda M, et al. Review of bioactive molecules production, biomass, and basidiomata of shiitake culinary-medicinal mushrooms, Lentinula edodes (Agaricomycetes). Int J Med Mushrooms. 2019;21(9):841-850. https://doi.org/10.1615/IntJMedMushrooms.2019031849
  7. Shah SK, Walker PA, Moore-Olufemi SD, et al. An evidence-based review of a Lentinula edodes mushroom extract as complementary therapy in the surgical oncology patient. JPEN J Parenter Enteral Nutr. 2011;35(4):449-458. Jul https://doi.org/10.1177/0148607110380684
  8. Chang S, Miles P. Historical record of the early cultivation of Lentinula in China. Mushroom J Trop. 1987;7:31-37.
  9. Bohra A, Kilian B, Sivasankar S, et al. Reap the crop wild relatives for breeding future crops. Trends Biotechnol. 2022;40(4):412-431. https://doi.org/10.1016/j.tibtech.2021.08.009
  10. Renzi JP, Coyne CJ, Berger J, et al. How could the use of crop wild relatives in breeding increase the adaptation of crops to marginal environments? Front Plant Sci. 2022;13:886162.
  11. Wu L, van Peer A, Song W, et al. Cloning of the Lentinula edodes B mating-type locus and identification of the genetic structure controlling B mating. Gene. 2013;531(2):270-278. https://doi.org/10.1016/j.gene.2013.08.090
  12. Ha BS, Moon YJ, Song Y, et al. Molecular analysis of B mating type diversity in Lentinula edodes. Sci Hortic. 2019;243:55-63.
  13. Au CH, Wong MC, Bao D, et al. The genetic structure of the A mating-type locus of Lentinula edodes. Gene. 2014;535(2):184-190. https://doi.org/10.1016/j.gene.2013.11.036
  14. Ha B, Kim S, Kim M, et al. Diversity of A mating type in Lentinula edodes and mating type preference in the cultivated strains. J Microbiol. 2018;56(6):416-425. https://doi.org/10.1007/s12275-018-8030-6
  15. Banham AH, Asante-Owusu RN, Gottgens B, et al. An N-terminal dimerization domain permits homeodomain proteins to choose compatible partners and initiate sexual development in the mushroom Coprinus cinereus. Plant Cell. 1995;7(6):773-783.
  16. James TY, Liou SR, Vilgalys R. The genetic structure and diversity of the a and B mating-type genes from the tropical oyster mushroom, Pleurotus djamor. Fungal Genet Biol. 2004;41(8):813-825. https://doi.org/10.1016/j.fgb.2004.04.005
  17. Wang W, Lian L, Xu P, et al. Advances in understanding mating type gene organization in the mushroom-forming fungus Flammulina velutipes. G3 (Bethesda). 2016;6(11):3635-3645. https://doi.org/10.1534/g3.116.034637
  18. Park YA, Seo S, Ka KH. Cultural characteristics and morphological comparison of the wild mushroom Lentinula edodes cultivated on sawdust substrate. Kor J Mycol. 2018;46(2):177-185.
  19. Schneider TD, Stephens RM. Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 1990;18(20):6097-6100. https://doi.org/10.1093/nar/18.20.6097
  20. Crooks GE, Hon G, Chandonia JM, et al. WebLogo: a sequence logo generator. Genome Res. 2004;14(6):1188-1190.
  21. Stothard P. The sequence manipulation suite: javaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques. 2000;28(6):1102-1104. https://doi.org/10.2144/00286ir01
  22. Pardo EH, O'Shea SF, Casselton LA. Multiple versions of the A mating type locus of Coprinus cinereus are generated by three paralogous pairs of multiallelic homeobox genes. Genetics. 1996;144(1):87-94. https://doi.org/10.1093/genetics/144.1.87
  23. Schirawski J, Heinze B, Wagenknecht M, et al. Mating type loci of Sporisorium reilianum: novel pattern with three A and multiple B specificities. Eukaryot Cell. 2005;4(8):1317-1327. https://doi.org/10.1128/EC.4.8.1317-1327.2005
  24. Gong WB, Liu W, Lu YY, et al. Constructing a new integrated genetic linkage map and mapping quantitative trait loci for vegetative mycelium growth rate in Lentinula edodes. Fungal Biol. 2014;118(3):295-308. https://doi.org/10.1016/j.funbio.2014.01.001
  25. 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. 2016;100(12):5437-5452. https://doi.org/10.1007/s00253-016-7347-5
  26. Zhang L, Gong W, Li C, et al. RNA-Seq-based high-resolution linkage map reveals the genetic architecture of fruiting body development in shiitake mushroom, Lentinula edodes. Comput Struct Biotechnol J. 2021;19:1641-1653. https://doi.org/10.1016/j.csbj.2021.03.016
  27. 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;15:37.
  28. Lee HY, Moon S, Ro HS, 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. https://doi.org/10.1080/12298093.2020.1727401
  29. Kurischko C, Schilhabel MB, Kunze I, et al. The MATA locus of the dimorphic yeast Yarrowia lipolytica consists of two divergently oriented genes. Mol Gen Genet. 1999;262(1):180-188. https://doi.org/10.1007/s004380051073
  30. Balasubramanian B, Lowry CV, Zitomer RS. The Rox1 repressor of the Saccharomyces cerevisiae hypoxic genes is a specific DNA-binding protein with a high-mobility-group motif. Mol Cell Biol. 1993;13(10):6071-6078. https://doi.org/10.1128/MCB.13.10.6071
  31. Gaur T, Lengner CJ, Hovhannisyan H, et al. Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2 gene expression. J Biol Chem. 2005;280(39):33132-33140. https://doi.org/10.1074/jbc.M500608200
  32. Choi H, Kim TH, Yang S, et al. A reciprocal interaction between β-Catenin and osterix in cementogenesis. Sci Rep. 2017;7(1):8160.
  33. Aras S, Maroun MC, Song Y, et al. Mitochondrial autoimmunity and MNRR1 in breast carcinogenesis. BMC Cancer. 2019;19(1):411.
  34. Lee SH, Ali A, Ha B, et al. Development of a molecular marker linked to the A4 locus and the structure of HD genes in Pleurotus eryngii. Mycobiology. 2019;47(2):200-206. https://doi.org/10.1080/12298093.2019.1619989