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The reversible degeneration of heat-treated Scenedesmus vacuolatus under continuous light cultivation conditions

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Abstract

To find out how microalgae cope with heat stress, the small vegetative cells of a synchronous Scenedesmus vacuolatus culture were subjected to heat treatment and then cultured under continuous illumination. The heat-treated cells were found first to enter a degenerative intermediate stage with low cellular activities almost right after the start of the cultivation, which was then followed by a revival. The changes in physiological activities and morphology of the treated cells throughout the whole period of regeneration were explored. The variations in cellular DNA content and protein composition were also investigated. Stressed cells at the end of the degeneration stage were completely bleached and were also characterized by condensed but undegraded chromatin, partially disintegrated chloroplasts but with the thylakoid membrane system retained, partially operating mitochondria, intact plasma membranes, and a dramatically changed profile of cellular proteins. All of our data indicate they were still alive but in a different physiological state than the control cells. Recovery started with regeneration of mitochondrial cristae and redispersion of chromatins. These were followed by regreening and resuscitation of chloroplasts, which often started from one part of a thylakoid membrane system and then spread out. This study provided a unicellular model for studying how plant cells react to a period of stress and recover.

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Abbreviations

2DE:

Two-dimensional gel electrophoresis

DAPI:

4′-6-Diamidino-2-phenylindole

MTT:

3-[4,5-Dimethylthiazol-2-yl]-2,5-diphenyl-tetrazolium bromide

PBS:

Phosphate buffered saline

ROS:

Reactive oxygen species

TEM:

Transmission electron microscopy

References

  • Affenzeller MJ, Darehshouri A, Andosch A, Lütz C, Lütz-Meindl U (2009) PCD and autophagy in the unicellular green alga Micrasterias denticulata. Autophagy 5:854–855

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550

    Article  CAS  PubMed  Google Scholar 

  • Becker EW (1994) Measurement of algal growth. In: Microalgae: biotechnology and Microbiology. Cambridge University Press, Cambridge, pp 56–62

    Google Scholar 

  • Berry JA, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543

    Article  Google Scholar 

  • Bumbulis MJ, Balog BM (2013) UV-C exposure induces an apoptosis-like process in Euglena gracilis. ISRN Cell Biol. doi:10.1155/2013/869216

    Google Scholar 

  • Cakmak I (2000) Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol 146:185–205

    Article  CAS  Google Scholar 

  • Cameron RE, Blank GB (1966) Desert algae: soil crusts and diaphanous substrata as algal habitats. In: Technical Report 32-971. Jet Propulsion Laboratory, California Institute of Technology, Pasadena, pp 1–41

  • Chen PC, Lai CL (1996) Physiological adaptation during cell dehydration and rewetting of a newly-isolated Chlorella species. Physiol Plant 96:453–457

    Article  CAS  Google Scholar 

  • Chen PC, Lorenzen H (1986) Changes in the productivity and nuclear divisions in synchronous Chlorella and circadian rhythm. Plant Cell Physiol 27:1423–1427

    CAS  Google Scholar 

  • Choi KM, Lee MY (2012) Differential protein expression associated with heat stress in Antarctic microalga. BioChip J 6:271–279

    Article  CAS  Google Scholar 

  • González A, Steffen KL, Lynch JP (1998) Light and excess manganese, implications for oxidative stress in common bean. Plant Physiol 118:493–504

    Article  PubMed Central  PubMed  Google Scholar 

  • Grossmann K, Kwiatkowski J, Tresch S (2001) Auxin herbicides induce H2O2 overproduction and tissue damage in cleavers (Galium aparine L.). J Exp Bot 52:1811–1816

    Article  CAS  PubMed  Google Scholar 

  • Houot V, Etienne P, Petitot AS, Barbier S, Blein JP, Suty L (2001) Hydrogen peroxide induces programmed cell death features in cultured tobacco BY-2 cells, in a dose-dependent manner. J Exp Bot 52:1721–1730

    Article  CAS  PubMed  Google Scholar 

  • Ikegawa H, Yamamoto Y, Matsumoto H (1998) Cell death caused by a combination of aluminum and iron in cultured tobacco cells. Physiol Plant 104:474–478

    Article  CAS  Google Scholar 

  • Inada N, Sakai A, Kuroiwa H, Kuroiwa T (1998) Three-dimensional analysis of the senescence program in rice (Oryza sativa L.) coleoptiles—investigations by fluorescence microscopy and electron microscopy. Planta 205:153–164

    Article  CAS  PubMed  Google Scholar 

  • Jiménez C, Capasso JM, Edelstein CL, Rivard CJ, Lucia S, Breusegem S, Berl T, Segovia M (2009) Different ways to die: cell death modes of the unicellular chlorophyte Dunaliella viridis exposed to various environmental stresses are mediated by the caspase-like activity DEVDase. J Exp Bot 60:815–828

    Article  PubMed Central  PubMed  Google Scholar 

  • Khanna-Chopra R (2012) Leaf senescence and abiotic stresses share reactive oxygen species-mediated chloroplast degradation. Protoplasma 249:469–481

    Article  CAS  PubMed  Google Scholar 

  • Krupinska K (2007) Fate and activities of plastids during leaf senescence. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, Dordrecht, pp 433–449

    Chapter  Google Scholar 

  • Lee TC, Hsu BD (2013) Characterization of the decline and recovery of heat-treated Scenedesmus vacuolatus. Bot Stud. doi:10.1186/1999-3110-54-3

    Google Scholar 

  • Matile P, Hörtensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Physiol Plant Mol Biol 50:67–95

    CAS  PubMed  Google Scholar 

  • Moharikar S, D’Souza JS, Kulkarni AB, Rao BJ (2006) Apoptotic-like cell death pathway is induced in unicellular chlorophyte Chlamydomonas reinhardtii (Chlorophyceae) cells following UV radiation: detection and functional analyses. J Phycol 42:423–433

    Article  CAS  Google Scholar 

  • Mühlhaus T, Weiss J, Hemme D, Sommer F, Schroda M (2011) Quantitative shotgun proteomics using a uniform 15N-labeled standard to monitor proteome dynamics in time course experiments reveals new insights into the heat stress response of Chlamydomonas reinhardtii. Mol Cell Proteomics. doi:10.1074/mcp.M110.004739

    PubMed Central  PubMed  Google Scholar 

  • Munné-Bosch S, Jubany-Marí T, Alegre L (2001) Drought-induced senescence is characterized by loss of antioxidant defences in chloroplasts. Plant Cell Environ 24:1319–1327

    Article  Google Scholar 

  • Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Annu Rev Plant Biol 54:329–355

    Article  PubMed  Google Scholar 

  • Schmollinger S, Schulz-Raffelt M, Strenkert D, Veyel D, Vallon O, Schroda M (2013) Dissecting the heat stress response in Chlamydomonas by pharmaceutical and RNAi approaches reveals conserved and novel aspects. Mol Plant 6:1795–1813

    Article  CAS  PubMed  Google Scholar 

  • Segovia M, Berges JA (2009) Inhibition of caspase-like activities prevents appearance of reactive oxygen species and dark-induced apoptosis in the unicellular chlorophyte Dunaliella tertiolecta. J Phycol 45:1116–1126

    Article  CAS  Google Scholar 

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51

    Article  CAS  Google Scholar 

  • van Doorn WG, Woltering EJ (2005) Many ways to exit? Cell death categories in plants. Trends Plant Sci 10:117–122

    Article  PubMed  Google Scholar 

  • van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, Mur LA, Petersen M, Smertenko A, Taliansky M, van Breusegem F, Wolpert T, Woltering E, Zhivotovsky B, Bozhkov PV (2011) Morphological classification of plant cell deaths. Cell Death Differ 18:1241–1246

    Article  PubMed Central  PubMed  Google Scholar 

  • Yamane K, Rahman MS, Kawasaki M, Taniguchi M, Miyake H (2004) Pretreatment with antioxidants decreases the effects of salt stress on chloroplast ultrastructure in rice leaf segments (Oryza sativa L.). Plant Prod Sci 7:292–300

    Article  CAS  Google Scholar 

  • Yordanov IS, Dilova R, Petkova T, Pangelova V, Goltsev V, Zuss KH (1986) Mechanisms of the temperature damage and acclimation of the photosynthetic apparatus. Photobiochem Photobiophys 12:147–155

    Google Scholar 

  • Zhang D, Koay ESC (2008) Analysis of laser capture microdissected cells by 2-dimensional gel electrophoresis. In: Vlahou A (ed) Clinical proteomics, methods and protocols. Humana Press, Totowa, pp 77–91

    Chapter  Google Scholar 

  • Zuppini A, Andreoli C, Baldan B (2007) Heat stress: an inducer of programmed cell death in Chlorella saccharophila. Plant Cell Physiol 48:1000–1009

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Council of Taiwan [NSC 97-2311-B-007 -002].

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Life Science, National Tsing Hua University, No. 101, Section 2, Kuang-Fu Road, Hsinchu, 30013, Taiwan

    Tzan-Chain Lee & Ban-Dar Hsu

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  1. Tzan-Chain Lee
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  2. Ban-Dar Hsu
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Correspondence to Ban-Dar Hsu.

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Handling Editor: Andreas Holzinger

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Lee, TC., Hsu, BD. The reversible degeneration of heat-treated Scenedesmus vacuolatus under continuous light cultivation conditions. Protoplasma 251, 1201–1211 (2014). https://doi.org/10.1007/s00709-014-0627-y

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  • DOI: https://doi.org/10.1007/s00709-014-0627-y

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