Abstract
High temperature is an important environmental factor that affects the growth and development of most edible fungi, however, the mechanism(s) for resistance to high temperature remains elusive. Nitric oxide is known to be able to effectively alleviate oxidative damage and plays an important role in the regulation of trehalose accumulation during heat stress in mycelia of Pleurotus eryngii var. tuoliensis. In this paper, we investigated whether heat stress can activate apoptosis-like cell death in mycelia of Pleurotus. Two Pleurotus species were used to detect morphological features characteristic of apoptosis including nuclear condensation, reactive oxygen species accumulation, and DNA fragmentation when exposed to heat stress (42 °C). The results showed that these classical apoptosis markers were apparent in Pleurotus strains after heat treatment. The heat-induced apoptosis-like cell death in Pleurotus was further probed using oligomycin and N-acetylcysteine, both of which were shown to block processes leading to apoptosis. This is the first report that apoptosis-like cell death occurs in Pleurotus species as a result of abiotic stress, and that this process can be inhibited with chemicals that block mitochondrial-induced apoptotic pathways and/or with ROS-scavenging compounds.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Azevedo MM, Almeida B, Ludovico P, Cássio F (2009) Metal stress induces programmed cell death in aquatic fungi. Aquat Toxicol 92(4):264–270
Chang ST, Miles PG (2004) Mushrooms: cultivation, nutritional value, medicinal effect, and environmental impact, 2nd edn. CRC Press, Florida
Chang ST, Wasser SP (2012) The role of culinary-medicinal mushrooms on human welfare with a pyramid model for human health. Int J Med Mushrooms 14(2):95–134
Chen C, Dickman MB (2005) Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc Natl Acad Sci USA 102(9):3459
Cheng J, Park TS, Chio LC, Fischl AS, Ye XS (2003) Induction of apoptosis by sphingoid long-chain bases in Aspergillus nidulans. Mol Cell Biol 23(1):163
Cohen R, Persky L, Hadar Y (2002) Biotechnological applications and potential of wood-degrading mushrooms of the genus Pleurotus. Appl Microbiol Biot 58(5):582–594
Dinamarco TM, Goldman MHS, Goldman GH (2011) Farnesol-induced cell death in the filamentous fungus Aspergillus nidulans. Biochem Soc Trans 39(5):1544
Emri T, Molnár Z, Pócsi I (2005) The appearances of autolytic and apoptotic markers are concomitant but differently regulated in carbon-starving Aspergillus nidulans cultures. FEMS Microbiol Lett 251(2):297–303
Fuchs Y, Steller H (2011) Programmed cell death in animal development and disease. Cell 147(4):742–758
Gourlay CW, Du W, Ayscough KR (2006) Apoptosis in yeast-mechanisms and benefits to a unicellular organism. Mol Microbiol 62(6):1515–1521
Hamann A, Brust D, Osiewacz HD (2008) Apoptosis pathways in fungal growth, development and ageing. Trends Microbiol 16(6):276–283
Harris SD, Morrell JL, Hamer JE (1994) Identification and characterization of Aspergillus nidulans mutants defective in cytokinesis. Genetics 136(2):517–532
Ito S, Ihara T, Tamura H, Tanaka S, Ikeda T, Kajihara H, Dissanayake C, Abdel-Motaal FF, El-Sayed MA (2007) α-Tomatine, the major saponin in tomato, induces programmed cell death mediated by reactive oxygen species in the fungal pathogen Fusarium oxysporum. FEBS Lett 581(17):3217–3222
Kong WW, Huang CY, Chen Q, Zou YJ, Zhang JX (2012) Nitric oxide alleviates heat stress-induced oxidative damage in Pleurotus eryngii var. tuoliensis. Fungal Genet Biol 49(1):15–20
Kong WW, Huang CY, Chen Q, Zou YJ, Zhao MR, Zhang JX (2012) Nitric oxide is involved in the regulation of trehalose accumulation under heat stress in Pleurotus eryngii var. tuoliensis. Biotechnol Lett 34(10):1915–1919
Leiter E, Szappanos H, Oberparleiter C, Kaiserer L, Csernoch L, Pusztahelyi T, Emri T, Pócsi I, Salvenmoser W, Marx F (2005) Antifungal protein PAF severely affects the integrity of the plasma membrane of Aspergillus nidulans and induces an apoptosis-like phenotype. Antimicrob Agents Chemother 49(6):2445
Lewis K (2000) Programmed death in bacteria. Microbiol Mol Biol Rev 64(3):503–514
Madeo F, Frohlich E, Frohlich KU (1997) A yeast mutant showing diagnostic markers of early and late apoptosis. J Cell Biol 139(3):729–734
Mousavi SAA, Robson GD (2004) Oxidative and amphotericin B-mediated cell death in the opportunistic pathogen Aspergillus fumigatus is associated with an apoptotic-like phenotype. Microbiology 150(6):1937–1945
Pawlik A, Janusz G, Koszerny J, Małek W, Rogalski J (2012) Genetic diversity of the edible mushroom Pleurotus sp. by amplified fragment length polymorphism. Curr Microbiol 65(4):438–445
Phillips AJ, Sudbery I, Ramsdale M (2003) Apoptosis induced by environmental stresses and amphotericin B in Candida albicans. Proc Natl Acad Sci USA 100(24):14327–14332
Qi G, Zhu F, Du P, Yang X, Qiu D, Yu Z, Chen J, Zhao X (2010) Lipopeptide induces apoptosis in fungal cells by a mitochondria-dependent pathway. Peptides 31(11):1978–1986
Reape TJ, McCabe PF (2008) Apoptotic-like programmed cell death in plants. New Phytol 180(1):13–26
Sánchez C (2009) Cultivation of Pleurotus ostreatus and other edible mushrooms. Appl Microbiol Biot 85(5):1321–1337
Sarangi I, Ghosh D, Bhutia SK, Mallick SK, Maiti TK (2006) Anti-tumor and immunomodulating effects of Pleurotus ostreatus mycelia-derived proteoglycans. Int Immunopharmacol 6(8):1287–1297
Semighini CP, Harris SD (2010) Methods to detect apoptotic-like cell death in filamentous fungi. Methods Mol Biol 638:269–279
Semighini CP, Hornby JM, Dumitru R, Nickerson KW, Harris SD (2006) Farnesol-induced apoptosis in Aspergillus nidulans reveals a possible mechanism for antagonistic interactions between fungi. Mol Microbiol 59(3):753–764
Semighini CP, Murray N, Harris SD (2008) Inhibition of Fusarium graminearum growth and development by farnesol. FEMS Microbiol Lett 279(2):259–264
Sharon A, Finkelstein A, Shlezinger N, Hatam I (2009) Fungal apoptosis: function, genes and gene function. FEMS Microbiol Rev 33(5):833–854
Vilgalys R, Sun BL (1994) Ancient and recent patterns of geographic speciation in the oyster mushroom Pleurotus revealed by phylogenetic analysis of ribosomal DNA sequences. Proc Natl Acad Sci USA 91(10):4599–4603
Acknowledgments
This work was supported by China Agriculture Research System (CARS24) and the National Natural Science Foundation of China (No. 31201667). We thank Ling Jiang for her assistance with use of the confocal laser scanning microscopy. We also thank Dr. Nemat O. Keyhani for reading and editing this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Song, C., Chen, Q., Wu, X. et al. Heat Stress Induces Apoptotic-Like Cell Death in Two Pleurotus Species. Curr Microbiol 69, 611–616 (2014). https://doi.org/10.1007/s00284-014-0634-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-014-0634-4