Mycobiology

The Korean Society of Mycology (한국균학회)
권호 표지
DOI QR코드

DOI QR Code

Cloning and Expression Analysis of Bioluminescence Genes in Omphalotus guepiniiformis Reveal Stress-Dependent Regulation of Bioluminescence

  • 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) ;
  • Min-Jun Kim (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) ;
  • Rhim, Ryoo (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 : 2023.08.29
  • Accepted : 2024.01.03
  • Published : 2024.01.31
Download PDF
⟨ Previous Next ⟩

Abstract

Bioluminescence is a type of chemiluminescence that arises from a luciferase-catalyzed oxidation reaction of luciferin. Molecular biology and comparative genomics have recently elucidated the genes involved in fungal bioluminescence and the evolutionary history of their clusters. owever, most studies on fungal bioluminescence have been limited to observing the changes in light intensity under various conditions. o understand the molecular basis of bioluminescent responses in Omphalotus guepiniiformis under different environmental conditions, we cloned and sequenced the genes of hispidin synthase, hispidin-3-hydroxylase, and luciferase enzymes, which are pivotal in the fungal bioluminescence pathway. ach gene showed high sequence similarity to that of other luminous fungal species. Furthermore, we investigated their transcriptional changes in response to abiotic stresses. Wound stress enhanced the bioluminescence intensity by increasing the expression of bioluminescence pathway genes, while temperature stress suppressed the bioluminescence intensity via the non-transcriptional pathway. Our data suggested that O. guepiniiformis regulates bioluminescence to respond differentially to specific environmental stresses. o our knowledge, this is the first study on fungal bioluminescence at the gene expression level. Further studies are required to address the biological and ecological meaning of different bioluminescence responses in changing environments, and O. quepiniiformis could be a potential model species.

Keywords

Acknowledgement

This work was supported by a grant from the General Project (FP0800-2023-01) provided by the National Institute of Forest Science, Republic of Korea.

References

  1. Wilson T, Hastings JW. Bioluminescence. Annu Rev Cell Dev Biol. 1998;14(1):197-230. doi: 10.1146/annurev.cellbio.14.1.197.
  2. Haddock SH, Moline MA, Case JF. Bioluminescence in the sea. Ann Rev Mar Sci. 2010;2(1):443-493. doi: 10.1146/annurev-marine-120308-081028.
  3. Oba Y, Schultz DT. Eco-evo bioluminescence on land and in the sea. Adv Biochem Eng Biotechnol. 2014;144:3-36. doi: 10.1007/978-3-662-43385-0_1.
  4. Kahlke T, Umbers KDL. Bioluminescence. Curr Biol. 2016;26(8):R313-4. doi: 10.1016/j.cub.2016.01.007.
  5. Lau ES, Oakley TH. Multi-level convergence of complex traits and the evolution of bioluminescence. Biol Rev Camb Philos Soc. 2021;96(2):673-691. doi: 10.1111/brv.12672.
  6. Syed A, Anderson JC. Applications of bioluminescence in biotechnology and beyond. Chem Soc Rev. 2021;50(9):5668-5705. doi: 10.1039/d0cs01492c.
  7. Tsarkova AS. Luciferins under construction: a review of known biosynthetic pathways. Front Ecol Evol. 2021;9:667829. doi: 10.3389/fevo.2021.667829.
  8. Ke HM, Tsai IJ. Understanding and using fungal bioluminescence - recent progress and future perspectives. Curr Opin Green Sustain Chem. 2022;33:100570. doi: 10.1016/j.cogsc.2021.100570.
  9. Purtov KV, Petushkov VN, Baranov MS, et al. The chemical basis of fungal bioluminescence. Angew Chem Int Ed Engl. 2015;54(28):8124-8128. doi: 10.1002/anie.201501779.
  10. Kotlobay AA, Sarkisyan KS, Mokrushina YA, et al. Genetically encodable bioluminescent system from fungi. Proc Natl Acad Sci U S A. 2018;115(50):12728-12732. doi: 10.1073/pnas.1803615115.
  11. Ke HM, Lee HH, Lin CYI, et al. Mycena genomes resolve the evolution of fungal bioluminescence. Proc Natl Acad Sci U S A. 2020;117(49):31267-31277. doi: 10.1073/pnas.2010761117.
  12. Kim JW, Park MJ, Shim DH, et al. De novo genome assembly of the bioluminescent mushroom Omphalotus guepiniiformis reveals an Omphalotus-specific lineage of the luciferase gene block. Genomics. 2022;114 (6):110514. doi: 10.1016/j.ygeno.2022.110514.
  13. Khakhar A, Starker CG, Chamness JC, et al. Building customizable auto-luminescent luciferase-based reporters in plants. Elife. 2020;9:e52786. doi: 10.7554/eLife.52786.
  14. Mitiouchkina T, Mishin AS, Somermeyer LG, et al. Plants with genetically encoded autoluminescence. Nat Biotechnol. 2020;38(8):944-946. doi: 10.1038/s41587-020-0500-9.
  15. Bermudes D, Petersen RH, Nealson KH. NealsonKH. Low-level bioluminescence detected in Mycena haematopus basidiocarps. Mycologia. 1992;84(5):799-802. doi: 10.1080/00275514.1992.12026208.
  16. Niitsu H, Hanyuda N, Sugiyama Y. Cultural properites of a luminous mushroom, Mycena chlorophos. Mycoscience. 2000;41(6):551-558. doi: 10.1007/BF02460920.
  17. Weitz HJ, Ballard AL, Campbell CD, et al. The effect of culture conditions on the mycelial growth and luminescence of naturally bioluminescent fungi. FEMS Microbiol Lett. 2001;202(2):165-170. doi: 10.1111/j.1574-6968.2001.tb10798.x.
  18. Mendes LF, Bastos EL, Desjardin DE, et al. Influence of culture conditions on mycelial growth and bioluminescence of Gerronema viridilucens. FEMS Microbiol Lett. 2008;282(1):132-139. doi: 10.1111/j.1574-6968.2008.01118.x.
  19. Medvedeva SE, Artemenko KS, Krivosheenko AA, et al. Growth and light emission of luminous basidiomycetes cultivated on solid media and in submerged culture. Mycosphere. 2014;5(4):565-577. doi: 10.5943/mycosphere/5/4/9.
  20. Ventura FF, Soares DMM, Bayle K, et al. Toxicity of metal cations and phenolic compounds to the bioluminescent fungus Neonothopanus gardneri. Environ Adv. 2021;4:100044. doi: 10.1016/j.envadv.2021.100044.
  21. Mihail JD, Bilyeu L, Lalk SR. Bioluminescence expression during the transition from mycelium to mushroom in three North American Armillaria and Desarmillaria species. Fungal Biol. 2018;122(11):1064-1068. doi: 10.1016/j.funbio.2018.08.007.
  22. Oliveira AG, Stevani CV, Waldenmaier HE, et al. Circadian control sheds light on fungal bioluminescence. Curr Biol. 2015;25(7):964-968. doi: 10.1016/j.cub.2015.02.021.
  23. Isobe M, Uyakul D, Goto T. Lampteromyces bioluminescence - 1. Identification of riboflavin as the light emitter in the mushroom L. japonicus. J Biolumin Chemilumin. 1987;1(3):181-188. doi: 10.1002/bio.1170010306.
  24. Park MJ, Lee H, Ryoo R. Changes in bioluminescence of Omphalotus japonicus mycelia under environmental stress conditions. Kor J Mycol. 2020;48(4):381-388. doi: 10.4489/KJM.20200037.
  25. Oba Y, Suzuki Y, Martins GNR, et al. Identification of hispidin as a bioluminescent active compound and its recycling biosynthesis in the luminous fungal fruiting body. Photochem Photobiol Sci. 2017;16(9):1435-1440. doi: 10.1039/c7pp00216e.
  26. Desjardin DE, Oliveira AG, Stevani CV. Fungi bioluminescence revisited. Photochem Photobiol Sci. 2008;7(2):170-182. doi: 10.1039/b713328f.
  27. Pelkmans JF, Patil MB, Gehrmann T, et al. Transcription factors of Schizophyllum commune involved in mushroom formation and modulation of vegetative growth. Sci Rep. 2017;7(1):310. doi: 10.1038/s41598-017-00483-3.
  28. Wu T, Hu C, Xie B, et al. A single transcription factor (PDD1) determines development and yield of winter mushroom (Flammulina velutipes). Appl Environ Microbiol. 2019;85(24):e01735-19. doi: 10.1128/AEM.01735-19.
  29. Meng L, Lyu X, Shi L, et al. The transcription factor FvHmg1 negatively regulates fruiting body development in winter mushroom Flammulina velutipes. Gene. 2021;785:145618. doi: 10.1016/j.gene.2021.145618.
  30. Ding Q, Zhao H, Zhu P, et al. Genome-wide identification and expression analyses of C2H2 zinc finger transcription factors in Pleurotus ostreatus. PeerJ. 2022;10:e12654. doi: 10.7717/peerj.12654.
  31. Lyu X, Wang Q, Liu A, et al. The transcription factor Ste12-like increases the mycelial abiotic stress tolerance and regulates the fruiting body development of Flammulina filiformis. Front Microbiol. 2023;14:1139679. doi: 10.3389/fmicb.2023.1139679.
  32. Sivinski JM. Arthropods attracted to luminous fungi. Psyche. 1981;88(3-4):383-390. doi: 10.1155/1981/79890.
  33. De Magalhaes Filho CD, Henriquez B, Seah NE, et al. Visible light reduces C. elegans longevity. Nat Commun. 2018;9(1):927. doi: 10.1038/s41467-018-02934-5.
  34. Xing YM, Zhang LC, Liang HQ, et al. Sclerotial formation of Polyporus umbellatus by low temperature treatment under artificial conditions. PLOS One. 2013;8(2):e56190. doi: 10.1371/journal.pone.0056190.
  35. Liu R, Zhang X, Ren A, et al. Heat stress-induced reactive oxygen species participate in the regulation of HSP expression, hyphal branching and ganoderic acid biosynthesis in Ganoderma lucidum. Microbiol Res. 2018;209:43-54. doi: 10.1016/j.micres.2018.02.006.
  36. Lei M, Wu X, Huang C, et al. Trehalose induced by reactive oxygen species relieved the radial growth defects of Pleurotus ostreatus under heat stress. Appl Microbiol Biotechnol. 2019;103(13):5379-5390. doi: 10.1007/s00253-019-09834-8.
  37. Iwahashi H, Ishii T, Sugata R, et al. The effects of caffeic acid and its related catechols on hydroxyl radical formation by 3-hydroxyanthranilic acid, ferric chloride, and hydrogen peroxide. Arch Biochem Biophys. 1990;276(1):242-247. doi: 10.1016/0003-9861(90)90033-u.
  38. Park IH, Chung SK, Lee KB, et al. An antioxidant hispidin from the mycelial cultures of Phellinus linteus. Arch Pharm Res. 2004;27(6):615-618. doi: 10.1007/BF02980159.
  39. Gulcin I. Antioxidant activity of caffeic acid (3,4-dihydroxycinnamic acid). Toxicology. 2006;217(2-3):213-220. doi: 10.1016/j.tox.2005.09.011.
  40. Chen W, Shen Y, Su H, et al. Hispidin derived from Phellinus linteus affords protection against acrylamide-induced oxidative stress in caco-2 cells. Chem Biol Interact. 2014;219:83-89. doi: 10.1016/j.cbi.2014.05.010.
  41. Ka KH, Park H, Hur TC, et al. Formation of fruiting body of Omphalotus japonicus by sawdust cultivation. Kor J Mycol. 2010;38(1):80-82. doi: 10.4489/KJM.2010.38.1.080.