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Effect of heat stress on actin cytoskeleton and endoplasmic reticulum of tobacco BY-2 cultured cells and its inhibition by Co2+

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Abstract

Temperature stress such as heat, cold, or freezing is a principal cause for yield reduction in crops. In particular, heat stress is very common and dangerous for plants since this stress can impact several plant and cellular functions. In spite of their role in sensing local stress and in controlling fundamental processes including PCD, the responses of cellular structures and organelles to heat stress are poorly investigated. In this work, we investigated the possible changes induced by mild heat stress, medium heat stress, and heat shock (HS; 5 min at 35°C, 45°C, or 50°C, respectively) on actin cytoskeleton and endoplasmic reticulum (ER) of tobacco BY-2 cultured cells. While mild and medium heat stresses are ineffective, HS induces depolymerization of actin microfilaments and changes in ER morphology accompanied by accumulation of the HSP70 binding protein (BiP). These effects of HS are prevented by the inhibitor of ethylene production Co2+. While the analyzed cell structures do not seem to be involved in the establishment of mild and medium heat stresses at least in this experimental system, the strong modifications induced by the treatment at 50°C suggest that actin cytoskeleton and ER may be involved in the responses to HS. Besides, the inhibiting effect of Co2+ suggests a role for ethylene as a regulative molecule in the responses to HS here observed.

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Abbreviations

BiP:

Binding protein

DiOC6 :

3,3’-Dihexyloxacarbocyanine iodide

ER:

Endoplasmic reticulum

HS:

Heat shock

PCD:

Programmed cell death

References

  • Balk J, Leaver CJ, McCabe PF (1999) Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants. FEBS Lett 463:151–154

    Article  CAS  PubMed  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18

    Article  CAS  PubMed  Google Scholar 

  • Broekaert WF, Delauré SL, De Bolle MFC, Cammue BPA (2006) The role of ethylene in host-pathogen interactions. Annu Rev Phytopathol 44:393–416

    Article  CAS  PubMed  Google Scholar 

  • Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357

    Article  CAS  PubMed  Google Scholar 

  • Ferri KF, Kroemer G (2001) Organelle-specific initiation of cell death pathways. Nat Cell Biol 3:E255–E263

    Article  CAS  PubMed  Google Scholar 

  • Gourlay CW, Ayscough KR (2005) The actin cytoskeleton in ageing and apoptosis. FEMS Yeast Res 5:1193–1198

    Article  CAS  PubMed  Google Scholar 

  • Hall AE (2001) Crop responses to the environment. CRC, Boca Raton, FL

    Google Scholar 

  • Hays DB, Do JH, Mason RE, Morgan G, Finlayson SA (2007) Heat stress induced ethylene production in developing wheat grains induces kernel abortion and increased maturation in a susceptible cultivar. Plant Sci 172:1113–1123

    Article  CAS  Google Scholar 

  • Hepler PK, Gunning BES (1998) Confocal fluorescence microscopy of plant cell. Protoplasma 201:121–157

    Article  Google Scholar 

  • Hussey PJ, Ketelaar T, Deeks MJ (2006) Control of the actin cytoskeleton in plant cell growth. Annu Rev Plant Biol 57:109–125

    Article  CAS  PubMed  Google Scholar 

  • Kampinga HH, Brunsting JF, Stege GJ, Burgman PW, Konings AW (1995) Thermal protein denaturation and protein aggregation in cells made thermotolerant by various chemicals: role of heat shock proteins. Exp Cell Res 219:536–546

    Article  CAS  PubMed  Google Scholar 

  • Klassen S, Bugbee B (2004) Ethylene synthesis and sensitivity in crop plants. HortScience 39:1546–1552

    CAS  PubMed  Google Scholar 

  • Koehl J, Djulic A, Kirner V, Nguyen TT, Heiser I (2007) Ethylene is required for elicitin-induced oxidative burst but not for cell death induction in tobacco cell suspension cultures. J Plant Physiol 164:1555–1563

    Article  CAS  PubMed  Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf K-D (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

    Article  CAS  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 5:305–315

    Article  CAS  PubMed  Google Scholar 

  • Leborgne-Castel N, Jelitto-Van Dooren EPWM, Crofts AJ, Denecke J (1999) Overexpression of BiP in tobacco alleviates endoplasmic reticulum stress. Plant Cell 11:459–469

    Article  CAS  PubMed  Google Scholar 

  • Locato V, Gadaleta C, Vacca RA, De Gara L, de Pinto MC (2008) Production of reactive species and modulation of antioxidant network in response to heat shock: a critical balance for cell fate. Plant Cell Environ 31:1606–1619

    Article  CAS  PubMed  Google Scholar 

  • Locato V, de Pinto MC, De Gara L (2009) Different involvement of mitochondrial, plastidial and cytosolic ascorbate-glutathione redox enzymes in heat shock responses. Physiol Plant 135:296–306

    Article  CAS  PubMed  Google Scholar 

  • Malerba M, Cerana R, Crosti P (2004) Comparison between the effects of fusicoccin, Tunicamycin, and Brefeldin A on programmed cell death of cultured sycamore (Acer pseudoplatanus L.) cells. Protoplasma 224:61–70

    CAS  PubMed  Google Scholar 

  • Malerba M, Contran N, Tonelli M, Crosti P, Cerana R (2008) Role of nitric oxide in actin depolymerization and programmed cell death induced by fusicoccin in sycamore (Acer pseudoplatanus L.) cultured cells. Physiol Plant 133:449–457

    Article  CAS  PubMed  Google Scholar 

  • McCabe PF, Leaver CJ (2000) Programmed cell death in cell cultures. Plant Mol Biol 44:359–368

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  CAS  PubMed  Google Scholar 

  • Müller J, Menzel D, Šamaj J (2007) Cell-type-specific disruption and recovery of the cytoskeleton in Arabidopsis thaliana epidermal root cells upon heat shock stress. Protoplasma 230:231–242

    Article  PubMed  Google Scholar 

  • Nagata T, Nemoto Y, Hasezawa S (1992) Tobacco BY-2 cell line as the ‘HeLa’ cell in the cell biology of higher plants. Int Rev Cytol 132:1–30

    Article  CAS  Google Scholar 

  • Nick P (2007) The plant cytoskeleton—new jobs for a versatile network. Protoplasma 230:125–127

    Article  CAS  PubMed  Google Scholar 

  • Oyadomari S, Araki E, Mori M (2002) Endoplasmic reticulum stress-mediated apoptosis in pancreatic beta-cells. Apoptosis 7:335–345

    Article  CAS  PubMed  Google Scholar 

  • Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646

    Article  CAS  PubMed  Google Scholar 

  • Sabnis RW, Deligeorgiev TG, Jachak MN, Dalvi TS (1997) DiOC6: a useful dye for staining the endoplasmic reticulum. Biotech Histochem 72:253–258

    Article  CAS  PubMed  Google Scholar 

  • Scorrano L, Oakes SC, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T, Korsmeyer SJ (2003) BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 300:135–139

    Article  CAS  PubMed  Google Scholar 

  • Scott I, Logan DC (2008) Mitochondrial morphology transition is an early indicator of subsequent cell death in Arabidopsis. New Phytol 177:90–101

    CAS  PubMed  Google Scholar 

  • Smertenko AP, Bozhkov PV, Filonova LH, von Arnold S, Hussey PJ (2003) Re-organisation of the cytoskeleton during developmental programmed cell death in Picea abies embryos. Plant J 33:813–824

    Article  CAS  PubMed  Google Scholar 

  • Sparvoli F, Faoro F, Daminati MG, Ceriotti A, Bollini R (2000) Misfolding and aggregation of vacuolar glycoproteins in plant cells. Plant J 24:825–836

    Article  CAS  PubMed  Google Scholar 

  • Storozhenko S, Pauw PD, Van Montagu M, Inze D, Kushnir S (1998) The heat-shock element is a functional component of the Arabidopsis APX1 gene promoter. Plant Physiol 118:1005–1014

    Article  CAS  PubMed  Google Scholar 

  • Suri SS, Dhindsa RS (2008) A heat-activated MAP kinase (HMAK) as activator of heat shock response in tobacco cells. Plant Cell Environ 31:218–226

    CAS  PubMed  Google Scholar 

  • Suzuki N, Rizhsky L, Bajad S, Liang H, Shuman J, Shulaev V, Mittler R (2005) Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiol 139:1313–1322

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Bajad S, Shuman J, Shulaev S, Mittler R (2008) The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. J Biol Chem 283:9269–9275

    Article  CAS  PubMed  Google Scholar 

  • Thomas SG, Huang S, Li S, Staiger CJ, Franklin-Tong VE (2006) Actin depolymerization is sufficient to induce programmed cell death in self-incompatible pollen. J Cell Biol 174:221–229

    Article  CAS  PubMed  Google Scholar 

  • Vacca RA, de Pinto MC, Valenti D, Passarella S, Marra E, De Gara L (2004) Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco Bright-Yellow 2 cells. Plant Physiol 134:1100–1112

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  CAS  PubMed  Google Scholar 

  • Watanabe N, Che FS, Iwano M, Takayama S, Nakano T, Yoshida S, Isogai A (1998) Molecular characterization of photomixotrophic tobacco cells resistant to protoporphyrinogen oxidase-inhibiting herbicides. Plant Physiol 118:751–758

    Article  CAS  PubMed  Google Scholar 

  • Wu C (1995) Heat shock transcription factors: structure and regulation. Annu Rev Cell Dev Biol 11:441–469

    Article  CAS  PubMed  Google Scholar 

Download references

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Correspondence to Massimo Malerba.

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Malerba, M., Crosti, P. & Cerana, R. Effect of heat stress on actin cytoskeleton and endoplasmic reticulum of tobacco BY-2 cultured cells and its inhibition by Co2+ . Protoplasma 239, 23–30 (2010). https://doi.org/10.1007/s00709-009-0078-z

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