Mycobiology

The Korean Society of Mycology (한국균학회)
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Activation of the Mating Pheromone Response Pathway of Lentinula edodes by Synthetic Pheromones

  • Ha, Byeongsuk (Division of Applied Life Science and Research Institute of Life Sciences, Gyeongsang National University) ;
  • Kim, Sinil (Division of Applied Life Science and Research Institute of Life Sciences, Gyeongsang National University) ;
  • Kim, Minseek (Division of Applied Life Science and Research Institute of Life Sciences, Gyeongsang National University) ;
  • Ro, Hyeon-Su (Division of Applied Life Science and Research Institute of Life Sciences, Gyeongsang National University)
  • Received : 2018.08.03
  • Accepted : 2018.10.23
  • Published : 2018.12.31
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Abstract

Pheromone (PHB)-receptor (RCB) interaction in the mating pheromone response pathway of Lentinula edodes was investigated using synthetic PHBs. Functionality of the C-terminally carboxymethylated synthetic PHBs was demonstrated by concentration-dependent induction of a mating-related gene (znf2) expression and by pseudoclamp formation in a monokaryotic strain S1-11 of L. edodes. Treatment with synthetic PHBs activated the expression of homeodomain genes (HDs) residing in the A mating type locus, and of A-regulated genes, including znf2, clp1, and priA, as well as genes in the B mating type locus, including pheromone (phb) and receptor (rcb) genes. The synthetic PHBs failed to discriminate self from non-self RCBs. PHBs of the B4 mating type (B4 PHBs) were able to activate the mating pheromone response pathway in both monokaryotic S1-11 and S1-13 strains, whose B mating types were B4 (self) and B12 (non-self), respectively. The same was true for B12 PHBs in the B4 (non-self) and B12 (self) mating types. The synthetic PHBs also promoted the mating of two monokaryotic strains carrying B4-common incompatible mating types ($A5B4{\times}A1B4$). However, the dikaryon generated by this process exhibited abnormally high content of hyphal branching and frequent clamp connections and, more importantly, was found to be genetically unstable due to overexpression of mating-related genes such as clp1. Although synthetic PHBs were unable to discriminate self from non-self RCBs, they showed a higher affinity for non-self RCBs, through which the mating pheromone response pathway in non-self cells may be preferentially activated.

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References

  1. Raudaskoski M, Kothe E. Basidiomycete mating type genes and pheromone signaling. Eukaryot Cell. 2010;9:847-859. https://doi.org/10.1128/EC.00319-09
  2. Kues U. From two to many: multiple mating types in Basidiomycetes. Fungal Biol Rev. 2015;29:126-166. https://doi.org/10.1016/j.fbr.2015.11.001
  3. Park H-O, Bi E. Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol Mol Biol Rev. 2007;71:48-96. https://doi.org/10.1128/MMBR.00028-06
  4. Bardwell L, Cook JG, Inouye CJ, et al. Signal propagation and regulation in the mating pheromone response pathway of the yeast Saccharomyces cerevisiae. Dev Biol. 1994;166:363-379. https://doi.org/10.1006/dbio.1994.1323
  5. Tam A, Nouvet FJ, Fujimura-Kamada K, et al. Dual roles for Ste24p in yeast a-factor maturation: NH2-terminal proteolysis and COOH-terminal CAAX processing. J Cell Biol. 1998;142:635-649. https://doi.org/10.1083/jcb.142.3.635
  6. Tam A, Schmidt WK, Michaelis S. The multispanning membrane protein Ste24p catalyzes CAAX proteolysis and NH2-terminal processing of the yeast a-factor precursor. J Biol Chem. 2001;276:46798-46806. https://doi.org/10.1074/jbc.M106150200
  7. Michaelis S, Barrowman J. Biogenesis of the Saccharomyces cerevisiae pheromone a-factor, from yeast mating to human disease. Microbiol Mol Biol Rev. 2012;76:626-651. https://doi.org/10.1128/MMBR.00010-12
  8. Hrycyna CA, Clarke S. Farnesyl cysteine C-terminal methyltransferase activity is dependent upon the STE14 gene product in Saccharomyces cerevisiae. Mol Cell Biol. 1990;10:5071-5076. https://doi.org/10.1128/MCB.10.10.5071
  9. He B, Chen P, Chen S-Y, et al. RAM2, an essential gene of yeast, and RAM1 encode the two polypeptide components of the farnesyltransferase that prenylates a-factor and Ras proteins. Proc Natl Acad Sci USA. 1991;88:11373-11377. https://doi.org/10.1073/pnas.88.24.11373
  10. Caldwell GA, Naider F, Becker JM. Fungal lipopeptide mating pheromones: a model system for the study of protein prenylation. Microbiol Rev. 1995;59:406-422.
  11. Casselton LA, Olesnicky NS. Molecular genetics of mating recognition in basidiomycete fungi. Microbiol Mol Biol Rev. 1998;62:55-70.
  12. Raper JR, Baxter MG, Ellingboe AH. The genetic structure of the incompatibility factors of Schizophyllum Commune: the A-factor. Proc Natl Acad Sci USA. 1960;46:833-842. https://doi.org/10.1073/pnas.46.6.833
  13. Riquelme M, Challen MP, Casselton LA, et al. The origin of multiple B mating specificities in Coprinus cinereus. Genetics. 2005;170:1105-1119. https://doi.org/10.1534/genetics.105.040774
  14. Fowler TJ, DeSimone SM, Mitton MF, et al. Multiple sex pheromones and receptors of a mushroom-producing fungus elicit mating in yeast. Mol Biol Cell. 1999;10:2559-2572. https://doi.org/10.1091/mbc.10.8.2559
  15. Fowler TJ, Mitton MF, Vaillancourt LJ, et al. Changes in mate recognition through alterations of pheromones and receptors in the multisexual mushroom fungus Schizophyllum commune. Genetics. 2001;158:1491-1503.
  16. Kues U. Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Rev. 2000;64:316-353. https://doi.org/10.1128/MMBR.64.2.316-353.2000
  17. Olesnicky NS, Brown AJ, Honda Y, et al. Selfcompatible B mutants in Coprinus with altered pheromone-receptor specificities. Genetics. 2000;156:1025-1033.
  18. Szabo Z, Tonnis M, Kessler H, et al. Structurefunction analysis of lipopeptide pheromones from the plant pathogen Ustilago maydis. Mol Genet Genom. 2002;268:362-370. https://doi.org/10.1007/s00438-002-0756-4
  19. Ha BS, Kim SI, Ro HS. Isolation and characterization of monokaryotic strains of Lentinula edodes showing higher fruiting rate and better fruiting body production. Mycobiology. 2015;43:24-30. https://doi.org/10.5941/MYCO.2015.43.1.24
  20. 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;56:416-425. https://doi.org/10.1007/s12275-018-8030-6
  21. Ha B, Moon YJ, Song Y, et al. Molecular analysis of B mating type diversity in Lentinula edodes. Sci Hortic. 2019;243:55-63. https://doi.org/10.1016/j.scienta.2018.08.009
  22. 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;531:270-278. https://doi.org/10.1016/j.gene.2013.08.090
  23. Kosted PJ, Gerhardt SA, Anderson CM, et al. Structural requirements for activity of the pheromones of Ustilago hordei. Fungal Genet Biol. 2000;29:107-117. https://doi.org/10.1006/fgbi.2000.1191
  24. Diaz-Rodriguez V, Distefano MD. a-Factor: a chemical biology tool for the study of protein prenylation. Curr Top Pept Protein Res. 2017;18:133-151.
  25. Olesnicky NS, Brown AJ, Dowell SJ, et al. A constitutively active G-protein-coupled receptor causes mating self-compatibility in the mushroom Coprinus. EMBO J. 1999;18:2756-2763. https://doi.org/10.1093/emboj/18.10.2756
  26. Heimel K, Scherer M, Vranes M, et al. The transcription factor Rbf1 is the master regulator for bmating type controlled pathogenic development in Ustilago maydis. PLoS Pathog. 2010;6:e1001035. https://doi.org/10.1371/journal.ppat.1001035
  27. Mead ME, Hull CM. Transcriptional control of sexual development in Cryptococcus neoformans. J Microbiol. 2016;54:339-346. https://doi.org/10.1007/s12275-016-6080-1
  28. Inada K, Morimoto Y, Arima T, et al. The clp1 gene of the mushroom Coprinus cinereus is essential for A-regulated sexual development. Genetics. 2001;157:133-140.
  29. O’Shea SF, Chaure PT, Halsall JR, et al. A large pheromone and receptor gene complex determines multiple B mating type specificities in Coprinus cinereus. Genetics. 1998;148:1081-1090.
  30. Halsall JR, Milner MJ, Casselton LA. Three subfamilies of pheromone and receptor genes generate multiple B mating specificities in the mushroom Coprinus cinereus. Genetics. 2000;154:1115-1123.
  31. Brown AJ, Casselton LA. Mating in mushrooms: increasing the chances but prolonging the affair. Trends Genet. 2001;17:393-400. https://doi.org/10.1016/S0168-9525(01)02343-5
  32. Yi R, Mukaiyama H, Tachikawa T, et al. A-mating type gene expression can drive clamp formation in the bipolar mushroom Pholiota microspore (Pholiota nameko). Eukaryot Cell. 2010;9:1109-1119. https://doi.org/10.1128/EC.00374-09
  33. Kajiwara S, Yamaoka K, Hori K, et al. Isolation and sequence of a developmentally regulated putative novel gene, priA, from the basidiomycete Lentinus edodes. Gene. 1992;114:173-178. https://doi.org/10.1016/0378-1119(92)90571-6

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