Skip to main content
SpringerLink
Log in

Salt stress-induced programmed cell death via Ca2+-mediated mitochondrial permeability transition in tobacco protoplasts

  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The change in cytosolic free concentration of calcium ([Ca2+]cyt) plays a key role in regulating apoptosis in animal cells. In our experiment, we tried to investigate the function of Ca2+ in programmed cell death (PCD) in tobacco (Nicotiana tobacum, cultivar BY-2) protoplasts induced by salt stress. An obvious increase in [Ca2+]cyt was observed a few minutes after treatment and the onset of a decrease in mitochondrial membrane potential (ΔΨm) was also observed before the appearance of PCD, pre-treatment of protoplasts with EGTA or LaCl3 effectively retarded the increase in [Ca2+]cyt, which was concomitant with the decrease in the percentage of cell death and higher ΔΨm, pre-treatment with cyclosporine A (CsA) also effectively retarded the increase in [Ca2+]cyt, the decrease in ΔΨm and the onset of PCD. All these results suggest that Ca2+ is a necessary element in regulating PCD and the increase in [Ca2+]cyt and the opening of mitochondrial permeability transition pore (MPTP) could promote each other in regulating PCD in tobacco protoplasts induced by salt stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AIF:

apoptosis inducing factor

ANT:

adenine nucleotide translocator

[Ca2+]cyt:

cytosolic free calcium concentration

CsA:

cyclosporin A

DCFH-DA:

2,7-dichlorohydrofluoroscein diacetate

EB:

ethidium bromide

HR:

hypersensitive response

MPTP:

mitochondrial permeability transition pore

PCD:

programmed cell death

PI:

propidium iodide

Rh123:

Rhodamine123

ROS:

reactive oxygen species

ΔΨm:

mitochondrial membrane potential

References

  • A. Ahad J. Wolf P. Nick (2003) ArticleTitleActivation-tagged tobacco mutants that are tolerant to antimicrotubular herbicides are cross-resistant to chilling stress Transgenic Res. 12 615–629 Occurrence Handle10.1023/A:1025814814823 Occurrence Handle14601660

    Article  PubMed  Google Scholar 

  • G.J. Allen S.P. Chu C.L. Harrington K. Schumacher T. Hoffmann Y.Y. Tang E. Grill J.I. Schroeder (2001) ArticleTitleA defined range of guard cell calcium oscillation parameters encodes stomatal movements Nature 411 1053–1057 Occurrence Handle10.1038/35082575 Occurrence Handle11429606

    Article  PubMed  Google Scholar 

  • S. Arpagaus A. Rawyler R. Braendle (2002) ArticleTitleOccurrence and characteristics of the mitochondrial permeability transition in plants J. Biol. Chem. 277 1780–1787 Occurrence Handle10.1074/jbc.M109416200 Occurrence Handle11704674

    Article  PubMed  Google Scholar 

  • C. Bergounioux S.C. Brown P.X. Petit (1992) ArticleTitleFlow cytometry and plant protoplast cell biology Physiol. Plant. 85 374–386 Occurrence Handle10.1034/j.1399-3054.1992.850236.x

    Article  Google Scholar 

  • S.L. Budd D.G. Nicholls (1996) ArticleTitleA re-evaluation of the role of mitochondria in neuronal calcium homeostasis J. Neurochem. 66 403–411 Occurrence Handle8522981

    PubMed  Google Scholar 

  • L.B. Chen (1988) ArticleTitleMitochondrial membrane potential in living cell Annu. Rev. Cell Biol. 4 155–181 Occurrence Handle10.1146/annurev.cb.04.110188.001103 Occurrence Handle3058159

    Article  PubMed  Google Scholar 

  • M.J. Curtis T.J. Wolpert (2002) ArticleTitleThe oat mitochondrial permeability transition and its implication in victorin binding and induced cell death Plant J. 29 295–312 Occurrence Handle10.1046/j.0960-7412.2001.01213.x Occurrence Handle11844107

    Article  PubMed  Google Scholar 

  • A. Danon V. Delorme N. Mailhac P. Gallois (2000) ArticleTitlePlant programmed celll death: a common way to dye Plant Physiol. Biochem. 38 647–655 Occurrence Handle10.1016/S0981-9428(00)01178-5

    Article  Google Scholar 

  • J.T. Greenberg A. Guo D.F. Klessig F.M. Ausubel (1994) ArticleTitleProgrammed cell death in plants: a pathogen-triggered response activitied coordinately with multiple defense function Cell 77 551–563 Occurrence Handle10.1016/0092-8674(94)90217-8 Occurrence Handle8187175

    Article  PubMed  Google Scholar 

  • J.B. Hoek J.L. Farber A.P. Thomas X. Wang (1995) ArticleTitleCalcium ion-dependent signalling and mitochondrial dysfunction: mitochondrial calcium uptake during hormonal stimulation in intact liver cells and its implication for the mitochondrial permeability transition Biochim. Biophys. Acta 1271 IssueID1 93–102 Occurrence Handle7599232

    PubMed  Google Scholar 

  • G.H. Huh B. Damsz T.K. Matsumoto M.P. Reddy A.M. Rus J.I. Ibeas M.L. Narasimhan R.A. Bressan P.M. Hasegawa (2002) ArticleTitleSalt causes ion disequilibrium-induced programmed cell death in yeast and plants Plant J. 29 649–659 Occurrence Handle10.1046/j.0960-7412.2001.01247.x Occurrence Handle11874577

    Article  PubMed  Google Scholar 

  • F. Ichas L.S. Jouaville J.P. Mazat (1997) ArticleTitleMitochondria are excitable organelles capable of generating and conveying electrical and calcium signals Cell 89 1145–1153 Occurrence Handle10.1016/S0092-8674(00)80301-3 Occurrence Handle9215636

    Article  PubMed  Google Scholar 

  • A. Ishihara H. Miyagawa Y. Kuwahara T. Ueno S. Mayama (1996) ArticleTitleInvolvement of Ca2+ ion in phytoalexin induction in oats Plant Sci. 115 9–16 Occurrence Handle10.1016/0168-9452(95)04322-5

    Article  Google Scholar 

  • A. Jones (2000) ArticleTitleDoes the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends Plant Sci. 5 225–230 Occurrence Handle10.1016/S1360-1385(00)01605-8 Occurrence Handle10785669

    Article  PubMed  Google Scholar 

  • R.N. Kao M.R. Michayluk (1975) ArticleTitleNutritional requirements for growth of Vicia hajastana cells at very low population density in liquid medium Planta 126 105–110 Occurrence Handle10.1007/BF00380613

    Article  Google Scholar 

  • G.E. Kass S. Orrenius (1999) ArticleTitleCalcium signaling and cytotoxicity Environ. Health Perspect. 107 IssueID(1 25–35 Occurrence Handle10229704

    PubMed  Google Scholar 

  • T. Kawano N. Sahashi K. Takahashi N. Uozumi S. Muto (1998) ArticleTitleSalicylic acid induces extracellular superoxide generation followed by an increase in cytosolic calcium ion in tobacco suspension culture: the earliest events in salicylic acid signal transudation Plant Cell Physiol. 39 721–730

    Google Scholar 

  • H. Knight A.J. Trewavas M.R. Knight (1996) ArticleTitleCold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation Plant Cell 8 IssueID3 489–503 Occurrence Handle10.1105/tpc.8.3.489 Occurrence Handle8721751

    Article  PubMed  Google Scholar 

  • G. Kroemer N. Zamzami S.A. Susin (1997) ArticleTitleMitochondrial control of apoptosis Immunol. Today 18 44–51 Occurrence Handle10.1016/S0167-5699(97)80014-X Occurrence Handle9018974

    Article  PubMed  Google Scholar 

  • A. Kuo S. Cappellutti M. Cervantes-Cervantes M. Rodriquez D.S. Bush (1996) ArticleTitleOkadaic acida protein phosphatase inhibitorblocks calcium changes, gene expression and cell death induced by gibberellin in wheat aleurone Plant Cell 8 259–269 Occurrence Handle10.1105/tpc.8.2.259 Occurrence Handle8742711

    Article  PubMed  Google Scholar 

  • C. Lacomme S. Santa Cruz (1999) ArticleTitleBax-induced cell death in tobacco is similar to the hypersensitive response Proc. Natl Acad. Sci. USA 96 7956–7961 Occurrence Handle10.1073/pnas.96.14.7956 Occurrence Handle10393929

    Article  PubMed  Google Scholar 

  • A.M. Lawrie R. Rizzuto T. Pozan A.W.M. Simpson (1996) ArticleTitleA role for calcium influx in the regulation of mitochondrial calcium in endothelial cells J. Biol. Chem. 271 10753–10759 Occurrence Handle10.1074/jbc.271.18.10753 Occurrence Handle8631885

    Article  PubMed  Google Scholar 

  • A. Levine R.I. Rennell M.E. Alvarez R. Palmer C. Lamb (1996) ArticleTitleCalcium-mediated apoptosis in a plant hypersensitive disease resistance response Curr. Biol. 6 IssueID4 427–437 Occurrence Handle10.1016/S0960-9822(02)00510-9 Occurrence Handle8723347

    Article  PubMed  Google Scholar 

  • J. Li D.Y. Wang Q. Li Y.J. Xu K.M. Cui Y.X. Zhu (2004) ArticleTitlePPF1 inhibits programmed cell death in apical meristems of both G2 pea and transgenic Arabidopsis plants possibly by delaying cytosolic Ca2+ elevation Cell Calcium 35 IssueID1 71–77 Occurrence Handle10.1016/j.ceca.2003.07.003 Occurrence Handle14670373

    Article  PubMed  Google Scholar 

  • E. Liljeroth T. Bryngelsson (2001) ArticleTitleDNA fragmentation in cereal roots indicative of programmed root cortical cell death Physiol. Plant. 111 363–372 Occurrence Handle10.1034/j.1399-3054.2001.1110314.x

    Article  Google Scholar 

  • X. Liu C.N. Kim J. Yang R. Jemmerson X. Wang (1996) ArticleTitleInduction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c Cell 86 147–157 Occurrence Handle1:CAS:528:DyaK28XktlGnsbY%3D Occurrence Handle8689682

    CAS  PubMed  Google Scholar 

  • T. Murashige F. Skoog (1962) ArticleTitleA revised medium for rapid growth and bioassay with tobacco tissue culture Physiol. Plant. 15 473–497

    Google Scholar 

  • L. Navazio P. Mariani D. Sanders (2001) ArticleTitleMobilization of Ca2+ by cyclic ADP-ribose from the endoplasmic reticulum of cauliflower florets Plant Physiol. 125 2129–2138 Occurrence Handle10.1104/pp.125.4.2129 Occurrence Handle11299392

    Article  PubMed  Google Scholar 

  • S. Orrenius B. Zhivotovsky P. Nicotera (2003) ArticleTitleRegulation of cell death: the calcium-apoptosis link Nature 4 552–565

    Google Scholar 

  • M.V. Rao K.R. Davis (1999) ArticleTitleOzone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid Plant J. 6 603–614 Occurrence Handle10.1046/j.1365-313X.1999.00400.x

    Article  Google Scholar 

  • C. Richter (1998) ArticleTitleNitric oxide and its congeners in mitochondria: implications for apoptosis Environ. Health Perspect. 106 1125–1128 Occurrence Handle9788886

    PubMed  Google Scholar 

  • D.E. Ryerson M.C. Heath (1996) ArticleTitleCleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments Plant Cell 8 393–402 Occurrence Handle10.1105/tpc.8.3.393 Occurrence Handle12239388

    Article  PubMed  Google Scholar 

  • E.E. Saviani C.H. Orsi J.F. Oliveira C.A. Pinto-Maglio I. Salgado (2002) ArticleTitleParticipation of the mitochondrial permeability transition pore in nitric oxide-induced plant cell death FEBS Lett. 510 136–140 Occurrence Handle10.1016/S0014-5793(01)03230-6 Occurrence Handle11801241

    Article  PubMed  Google Scholar 

  • D. Scheel (1998) ArticleTitleResistance response physiology and signal transduction Curr. Opin. Plant Biol. 1 IssueID4 305–310 Occurrence Handle10.1016/1369-5266(88)80051-7 Occurrence Handle10066609

    Article  PubMed  Google Scholar 

  • L. Scorrano S.A. Oakes J.T. Opferman E.H. Cheng M.D. Sorcinelli T. Pozan S.J. Korsmeyer (2003) ArticleTitleBAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis Science 300 135–139 Occurrence Handle10.1126/science.1081208 Occurrence Handle12624178

    Article  PubMed  Google Scholar 

  • P.B. Simpson J.T. Russell (1998) ArticleTitleRole of mitochondrial Ca2+ regulation in neuronal and glial cell signalling Brain Res. Rev. 26 72–82 Occurrence Handle10.1016/S0165-0173(97)00056-8 Occurrence Handle9600625

    Article  PubMed  Google Scholar 

  • S.S. Smaili Y. Hsu R.J. Youle J.T. Russell (2000) ArticleTitleMitochondria in Ca2+ signaling and apoptosis J. Bioenerg. Biomembr. 32 35–46 Occurrence Handle10.1023/A:1005508311495 Occurrence Handle11768760

    Article  PubMed  Google Scholar 

  • H. Steller (1995) ArticleTitleMechanisms and genes of cellular suicide Science 267 1445–1449 Occurrence Handle7878463

    PubMed  Google Scholar 

  • C.C. Subbaiah D.S. Bush M.M. Sachs (1998) ArticleTitleMitochondrial contribution to the anoxic Ca2+ signal in maize suspension-cultured cells Plant Physiol. 118 759–771 Occurrence Handle10.1104/pp.118.3.759 Occurrence Handle9808720

    Article  PubMed  Google Scholar 

  • S.G. Thomas V. Franklin-Tong (2004) ArticleTitleSelf-incompatibility triggers programmed cell death in Papaver pollen Nature 429 305–309 Occurrence Handle10.1038/nature02540 Occurrence Handle15152254

    Article  PubMed  Google Scholar 

  • H.L.A. Vieira G. Kroemer (1999) ArticleTitlePathophysiology of mitochondrial cell death control Cell. Mol. Life Sci. 56 971–976 Occurrence Handle10.1007/s000180050486 Occurrence Handle11212328

    Article  PubMed  Google Scholar 

  • C.Y. Wang J.H. Bowen I.E. Weir A.C. Allan I.B. Perguson (2001) ArticleTitleHeat-induced protection against death of suspension-cultured apple fruit cells exposed to low temperature Plant Cell Environ. 24 1199–1207 Occurrence Handle10.1046/j.1365-3040.2001.00770.x

    Article  Google Scholar 

  • R.J. White I.J. Reynolds (1996) ArticleTitleMitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure J Neurosci. 16 5688–5697 Occurrence Handle8795624

    PubMed  Google Scholar 

  • Z. Xie Z. Chen (2000) ArticleTitleHarpin-induced hypersensitive cell death is associated with altered mitochondrial functions in tobacco cells Mol. Plant–Microbe. Interact. 13 183–190 Occurrence Handle10659708

    PubMed  Google Scholar 

  • H.X. Xu M.C. Heath (1998) ArticleTitleRole of calcium in signal transudation during the hypersensitive response caused by basidiospore infection of the cowpea rust fungus Plant Cell. 10 585–597 Occurrence Handle10.1105/tpc.10.4.585 Occurrence Handle9548984

    Article  PubMed  Google Scholar 

  • Y. Yamamoto Y. Kobayashi S. Rama Devi S. Rikiishi H. Matsumoto (2002) ArticleTitleAluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells Plant Physiol. 128 63–72 Occurrence Handle10.1104/pp.128.1.63 Occurrence Handle11788753

    Article  PubMed  Google Scholar 

  • K. Yasuhiro F. Takuya O. Yoko G. Tatsuaki H. Katsumi M. Shoshi K. Kazuyuki (2004) ArticleTitleIdentification of putative voltage-dependent Ca2+-permeable channels involved in cryptogein-induced Ca2+ transients and defense responses in tobacco BY-2 cells Biochem. Biophys. Res. Commun. 317 823–828 Occurrence Handle10.1016/j.bbrc.2004.03.114 Occurrence Handle15081414

    Article  PubMed  Google Scholar 

  • X.H. Yu T.D. Perdue Y.M. Heimer A.M. Jones (2002) ArticleTitleMitochondrial involvement in tracheary element programmed cell death Cell Death Differ. 9 189–198 Occurrence Handle10.1038/sj/cdd/4400940 Occurrence Handle11840169

    Article  PubMed  Google Scholar 

  • M. Zoratti I. Szabo (1995) ArticleTitleThe mitochondrial permeability transition Biochim. Biophys. Acta 1241 139–176 Occurrence Handle7640294

    PubMed  Google Scholar 

  • A. Zuppini L. Navazio P. Mariani (2004) ArticleTitleEndoplasmic reticulum stress-induced programmed cell death in soybean cells J. Cell Sci. 117 IssueID12 2591–2598 Occurrence Handle10.1242/jcs.01126 Occurrence Handle15159454

    Article  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Jiusheng Lin

    Present address: Department of Biochemistry & Plant Science Initiative, University of Nebraska-Lincoln, Lincoln, NE, 68588, USA

Authors and Affiliations

  1. College of Life Sciences, Zhejiang University, Hanzhou, Zhejiang Province, 310029, China

    Jiusheng Lin & Genxuan Wang

  2. Key Laboratory of Arid Agroecology, Ministry of Education, Lanzhou University, Lanzhou, Gansu Province, 730000, China

    Jiusheng Lin & Yuan Wang

Authors
  1. Jiusheng Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Genxuan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jiusheng Lin.

Additional information

Jiusheng Lin and Yuan Wang-These authors contributed equally for this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lin, J., Wang, Y. & Wang, G. Salt stress-induced programmed cell death via Ca2+-mediated mitochondrial permeability transition in tobacco protoplasts. Plant Growth Regul 45, 243–250 (2005). https://doi.org/10.1007/s10725-005-5163-5

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-005-5163-5

Keywords

Search

Navigation