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Voltage-dependent anion channels: their roles in plant defense and cell death

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Abstract

The voltage-dependent anion channels (VDACs), mitochondrial outer membrane components, are present in organisms from fungi to animals and plants. They are thought to function in the regulation of metabolite transport between mitochondria and the cytoplasm. Sufficient knowledge on plant VDACs has been accumulated, so that we can here summarize the current information. Then, the involvement of mitochondria in plant defense and cell death is overviewed. While, in mammals, it is suggested that VDAC, also known as a component of the permeability transition pore (PTP) complex formed in the junction site of mitochondrial outer and inner membrane, is a key player in mitochondria-mediated cell death, little is known about the role of plant VDACs in this process. We have shown that plant VDACs are involved in mitochondria-mediated cell death and in defense against a non-host pathogen. In light of the current findings, we discuss the role of the PTP complex and VDAC as its component in plant pathogen defense and cell death.

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References

  • Adrain C, Martin SJ (2001) The mitochondrial apoptosome: a killer unleashed by the cytochrome seas. Trends Biochem Sci 26:390–397

    Article  PubMed  CAS  Google Scholar 

  • Al Bitar F, Roosens N, Boxtel JV, Dewaele E, Jacobs M, Homblé F (2002) Expression of the rice vdac isoform2: histochemical localization and expression level. Biochim Biophys Acta 1579:133–141

    PubMed  CAS  Google Scholar 

  • Al Bitar F, Roosens N, Smeyers M, Vauterin M, Van Boxtel J, Jacobs M, Homblé F (2003) Sequence analysis, transcriptional and posttranscriptional regulation of the rice vdac family. Biochim Biophys Acta 1625:43–51

    PubMed  CAS  Google Scholar 

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Aravind L, Dixit VM, Koonin EV (2001) Apoptotic molecular machinery: vastly increased complexity in vertebrates revealed by genome comparisons. Science 291:1279–1284

    Article  PubMed  CAS  Google Scholar 

  • Arpagaus S, Rawyler A, Braendle R (2002) Occurrence and characteristics of the mitochondrial permeability transition in plants. J Biol Chem 277:1780–1787

    Article  PubMed  CAS  Google Scholar 

  • Baek D, Nam J, Koo YD, Kim DH, Lee J, Jeong JC, Kwak SS, Chung WS, Lim CO, Bahk JD, Hong JC, Lee SY, Kawai-Yamada M, Uchimiya H, Yun DJ (2004) Bax-induced cell death of Arabidopsis is mediated through reactive oxygen-dependent and -independent processes. Plant Mol Biol 56:15–27

    Article  PubMed  CAS  Google Scholar 

  • Baines CP, Kaiser RA, Sheiko T, Craigen WJ, Molkentin JD (2007) Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol 9:550–555

    Article  PubMed  CAS  Google Scholar 

  • Balk J, Leaver CJ (2001) The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13:1803–1818

    Article  PubMed  CAS  Google Scholar 

  • Benz R (1994) Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins. Biochim Biophys Acta 1197:167–196

    PubMed  CAS  Google Scholar 

  • Brenner C, Grimm S (2006) The permeability transition pore complex in cancer cell death. Oncogene 25:4744–4756

    Article  PubMed  CAS  Google Scholar 

  • Buettner R, Papoutsoglou G, Scemes E, Spray DC, Dermietzel R (2000) Evidence for secretory pathway localization of a voltage-dependent anion channel isoform. Proc Natl Acad Sci USA 97:3201–3206

    Article  PubMed  CAS  Google Scholar 

  • Clausen C, Ilkavets I, Thompson R, Philippar K, Vojta A, Möhlmann T, Neuhaus E, Fulgosi H, Soll J (2004) Intracellular localization of VDAC proteins in plants. Planta 220:30–37

    Article  PubMed  CAS  Google Scholar 

  • Craigen WJ, Graham BH (2008) Genetic strategies for dissecting mammalian and Drosophila voltage-dependent anion channel functions. J Bioenerg Biomembr 40:207–212

    Article  PubMed  CAS  Google Scholar 

  • Curtis MJ, Wolpert TJ (2004) The victorin-induced mitochondrial permeability transition preceded cell shrinkage and biochemical markers of cell death, and shrinkage occurs loss of membrane integrity. Plant J 38:244–259

    Article  PubMed  CAS  Google Scholar 

  • Desai MK, Mishra RN, Verma D, Nair S, Sopory SK, Reddy MK (2006) Structural and functional analysis of a salt stress inducible gene encoding voltage dependent anion channel (VDAC) from pearl millet (Pennisetum glaucum). Plant Physiol Biochem 44:483–493

    Article  PubMed  CAS  Google Scholar 

  • Dickman MB, Oltersdorf T, Li W, Clements T, French R (2001) Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci USA 98:6957–6962

    Article  PubMed  CAS  Google Scholar 

  • Dihanich M, Suda K, Schatz G (1987) A yeast mutant lacking mitochondrial porin is respiratory-deficient, but can recover respiration with simultaneous accumulation of an 86-kd extramitochondrial protein. EMBO J 6:723–728

    PubMed  CAS  Google Scholar 

  • Douce R, Neuburger M (1999) Biochemical dissection of photorespiration. Curr Opin Plant Biol 2:214–222

    Article  PubMed  CAS  Google Scholar 

  • Elkeles A, Devos KM, Graur D, Zizi M, Breiman A (1995) Multiple cDNAs of wheat voltage-dependent anion channels (VDAC): isolation, different expression, mapping and evolution. Plant Mol Biol 29:109–124

    Article  PubMed  CAS  Google Scholar 

  • Ferri KS, Kroemer G (2001) Mitochondria—the suicide organelles. Bioessays 23:111–115

    Article  PubMed  CAS  Google Scholar 

  • Giegé P, Heazlewood JL, Roessner-Tunali U, Millar AH, Fernie AR, Leaver CJ, Sweetlove LJ (2003) Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell 15:2140–2151

    Article  PubMed  Google Scholar 

  • Godbole A, Varghese J, Sarin A, Mathew MK (2003) VDAC is conserved element of death pathways in plant and animal systems. Biochim Biophys Acta 1642:87–96

    Article  PubMed  CAS  Google Scholar 

  • Graham BH, Craigen WJ (2004) Genetic approaches to analyzing mitochondrial outer membrane permeability. Curr Top Dev Biol 59:87–117

    Article  PubMed  CAS  Google Scholar 

  • Graham JW, Williams TC, Morgan M, Fernie AR, Ratcliffe RG, Sweetlove LJ (2007) Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling. Plant Cell 19:3723–3738

    Article  PubMed  CAS  Google Scholar 

  • Hofius D, Tsitsigiannis DI, Jones JDG, Mundy J (2007) Inducible cell death in plant immunity. Semin Cancer Biol 17:166–187

    Article  PubMed  CAS  Google Scholar 

  • Hoogenboom BW, Suda K, Engel A, Fotiadis D (2007) The supramolecular assemblies of voltage-dependent anion channels in the native membrane. J Mol Biol 370:246–255

    Article  PubMed  CAS  Google Scholar 

  • Kawai M, Pan L, Reed JC, Uchimiya H (1999) Evolutionally conserved plant homologue of the Bax Inhibitor-1 (BI-1) gene capable of suppressing Bax-induced cell death in yeast. FEBS Lett 464:143–147

    Article  PubMed  CAS  Google Scholar 

  • Kawai-Yamada M, Jin L, Yoshinaga K, Hirata A, Uchimiya H (2001) Mammalian Bax-induced plant cell death can be down-regulated by overexpression of Arabidopsis Bax Inhibitor-1 (AtBI-1). Proc Natl Acad Sci USA 98:12295–12300

    Article  PubMed  CAS  Google Scholar 

  • Kawai-Yamada M, Ohori Y, Uchimiya H (2004) Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax, hydrogen peroxide and salicylic acid-induced cell death. Plant Cell 16:21–32

    Article  PubMed  CAS  Google Scholar 

  • Kawai-Yamada M, Saito Y, Jin L, Ogawa T, Kim K-M, Yu L-H, Tone Y, Hirata A, Umeda M, Uchimiya H (2005) A novel Arabidopsis gene causes Bax-like lethality in Saccharomyces cerevisiae. J Biol Chem 47:39468–39473

    Article  Google Scholar 

  • Kim M, Lim J-H, Ahn CS, Park K, Kim GT, Kim WT, Pai H-S (2006) Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana. Plant Cell 18:2341–2355

    Article  PubMed  CAS  Google Scholar 

  • Krause M, Durner J (2004) Harpin inactivates mitochondria in Arabidopsis suspension cells. Mol Plant Microbe Interact 17:131–139

    Article  PubMed  CAS  Google Scholar 

  • Kroemer G, Reed JC (2000) Mitochondrial control of cell death. Nat Med 6:513–519

    Article  PubMed  CAS  Google Scholar 

  • Kroemer G, Zamzami N, Susin SA (1997) Mitochondrial control of apoptosis. Immunol Today 18:44–51

    Article  PubMed  CAS  Google Scholar 

  • Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87:99–163

    Article  PubMed  CAS  Google Scholar 

  • Lacomme C, Roby D (1999) Identification of new early markers of the hypersensitive response in Arabidopsis thaliana. FEBS Lett 459:149–153

    Article  PubMed  CAS  Google Scholar 

  • Lacomme C, Santa Cruz S (1999) Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc Natl Acad Sci USA 96:7956–7961

    Article  PubMed  CAS  Google Scholar 

  • Lam E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411:848–853

    Article  PubMed  CAS  Google Scholar 

  • Lee AC, Xu X, Blachly-Dyson E, Forte M, Colombini M (1998) The role of yeast VDAC genes on the permeability of the mitochondrial outer membrane. J Membr Biol 161:173–181

    Article  PubMed  CAS  Google Scholar 

  • Lee SM, Hoang MHT, Han HJ, Kim HS, Lee K, Kim KE, Kim DH, Lee SY, Chung WS (2009) Pathogen inducible voltage-dependent anion channel (AtVDAC) isoforms are localized to mitochondria membrane in Arabidopsis. Mol Cell 27:321–327

    Article  CAS  Google Scholar 

  • Love AJ, Milner JJ, Sadanandom A (2008) Timing is everything: regulatory overlap in plant cell death. Trends Plant Sci 13:589–595

    Article  PubMed  CAS  Google Scholar 

  • Madesh M, Hajnóczky G (2001) VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release. J Cell Biol 155:1003–1016

    Article  PubMed  CAS  Google Scholar 

  • Mannella CA (1982) Structure of the outer mitochondrial membrane: ordered arrays of porelike subunits in outer-membrane fractions from Neurospora crassa mitochondria. J Cell Biol 94:680–687

    Article  PubMed  CAS  Google Scholar 

  • Matsumura H, Nirasawa S, Kiba A, Urasaki N, Saitoh H, Ito M, Kawai-Yamada M, Uchimiya H, Terauchi R (2003) Overexpression of Bax inhibitor suppresses the fungal elicitor-induced cell death in rice (Oryza sativa L) cells. Plant J 33:425–434

    Article  PubMed  CAS  Google Scholar 

  • Mitchell P, Moyle J (1965) Evidence discriminating between the chemical and the chemiosmotic mechanisms of electron transport phosphorylation. Nature 208:1205–1206

    Article  PubMed  CAS  Google Scholar 

  • Mitsuhara I, Malik KA, Miura M, Ohashi Y (1999) Animal cell-death suppressors Bcl-xL and Ced-9 inhibit cell death in tobacco plants. Curr Biol 9:775–778

    Article  PubMed  CAS  Google Scholar 

  • Mur LAJ, Kenton P, Lloyd A, Ougham H, Prats E (2008) The hypersensitive response; the centenary is upon us but how much do we know? J Exp Bot 59:501–520

    Article  PubMed  CAS  Google Scholar 

  • Reumann S, Bettermann M, Heldt HW (1997) Evidence for the presence of a porin in the membrane of glyoxysomes of caster bean. Plant Physiol 115:891–899

    PubMed  CAS  Google Scholar 

  • Roosens N, Al Bitar F, Jacobs M, Homble F (2000) Characterization of a cDNA encoding a rice mitochondrial voltage-dependent anion channel and its gene expression studied upon. Biochim Biophys Acta 1463:470–476

    Article  PubMed  CAS  Google Scholar 

  • Salinas T, Duchêne AM, Delage L, Nilsson S, Glaser E, Zaepfel M, Maréchal-Drouard L (2006) The voltage-dependent anion channel, a major component of the tRNA import machinery in plant mitochondria. Proc Natl Acad Sci USA 103:18362–18367

    Article  PubMed  CAS  Google Scholar 

  • Sampson MJ, Lovell RS, Craigen WJ (1997) The murine voltage-dependent anion channel gene family. Conserved structure and function. J Biol Chem 272:18966–18973

    Article  PubMed  CAS  Google Scholar 

  • Shimizu S, Narita M, Tsujimoto Y (1999) BcL-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399:483–487

    Article  PubMed  CAS  Google Scholar 

  • Shimizu S, Ide T, Yanagida T, Tsujimoto Y (2000) Electrophysiological study of a novel large pore formed by Bax and the voltage-dependent anion channel that is permeable to cytochrome c. J Biol Chem 275:12321–12325

    Article  PubMed  CAS  Google Scholar 

  • Shimizu S, Matsuoka Y, Shinohara Y, Yoneda Y, Tsujimoto Y (2001) Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells. J Cell Biol 152:237–250

    Article  PubMed  CAS  Google Scholar 

  • Shoshan-Barmatz V, Israelson A (2005) The voltage-dependent anion channel in endoplasmic/sarcoplasmic reticulum: characterization, modulation and possible function. J Membr Biol 204:57–66

    Article  PubMed  CAS  Google Scholar 

  • Shoshan-Barmatz V, Zalk R, Gincel D, Vardi N (2004) Cellular and subcellular localization of VDAC in cerebellum and its function in ER-mitochondria cross-talk. Biochim Biophys Acta 1657:105–114

    Article  PubMed  CAS  Google Scholar 

  • Shoshan-Barmatz V, Keinan N, Zaid H (2008) Uncovering the role of VDAC in the regulation of cell life and death. J Bioenerg Biomembr 40:183–191

    Article  PubMed  CAS  Google Scholar 

  • Sugiyama T, Shimizu S, Matsuoka Y, Yoneda Y, Tsujimoto Y (2002) Activation of mitochondrial voltage-dependent anion channel by a pro-apoptotic BH3-only protein Bim. Oncogene 21:4944–4956

    Article  PubMed  CAS  Google Scholar 

  • Swidzinski JA, Sweetlove LJ, Leaver CJ (2002) A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J 30:431–446

    Article  PubMed  CAS  Google Scholar 

  • Swidzinski JA, Leaver CJ, Sweetlove LJ (2004) A proteomic analysis of plant programmed cell death. Phytochemistry 65:1829–1838

    Article  PubMed  CAS  Google Scholar 

  • Tajeddine N, Galluzi L, Kepp O, Hangen E, Morselli E, Senovilla L, Araujo N, Pinna G, Larochette N, Zamzami N, Modjtahedi N, Harel-Bellan A, Kroemer G (2008) Hierarchial involvement of Bak, VDAC1 and Bax in cisplatin-induced cell death. Oncogene 27:4221–4232

    Article  PubMed  CAS  Google Scholar 

  • Tateda C, Yamashita K, Takahashi F, Kusano T, Takahashi Y (2009a) Plant voltage-dependent anion channels are involved in host defense against Pseudomonas cichorii and in Bax-induced cell death. Plant Cell Rep 28:41–51

    Article  PubMed  CAS  Google Scholar 

  • Tateda C, Yamashita K, Takahashi F, Kusano T, Takahashi Y (2009b) Plant voltage-dependent anion channels are involved in host defense against Pseudomonas cichorii and in Bax-induced cell death. Plant Cell Rep 28:1145

    Article  CAS  Google Scholar 

  • Tiwari BS, Belenghi B, Levine A (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol 128:1271–1281

    Article  PubMed  CAS  Google Scholar 

  • Tsujimoto Y, Shimizu S (2007) Role of the mitochondrial membrane permeability transition in cell death. Apoptosis 12:835–840

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Vianello A, Zancani M, Peresson C, Petrussa E, Casolo V, Krajňáková J, Patui S, Braidot E, Marci F (2007) Plant mitochondrial pathway leading to programmed cell death. Physiol Plant 129:242–252

    Article  CAS  Google Scholar 

  • Wandrey M, Trevaskis B, Brewin N, Udvardi MK (2004) Molecular and cell biology of a family of voltage-dependent anion channel porins in Lotus japonicus. Plant Physiol 134:182–193

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Xu Q, Reed JC (1998) Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol Cell 1:337–346

    Article  PubMed  CAS  Google Scholar 

  • Yao N, Greenberg JT (2006) Arabidopsis ACCELERATED CELL DEATH2 modulates programmed cell death. Plant Cell 18:397–411

    Article  PubMed  CAS  Google Scholar 

  • Yao N, Tada Y, Sakamoto M, Nakayashiki H, Park P, Tosa Y, Mayama S (2002) Mitochondrial oxidative burst involved in apoptotic response in oats. Plant J 30:567–579

    Article  PubMed  CAS  Google Scholar 

  • Yao N, Eisfelder BJ, Marvin J, Greenberg JT (2004) The mitochondrion—an organelle commonly involved in programmed cell death in Arabidopsis thaliana. Plant J 40:596–610

    Article  PubMed  CAS  Google Scholar 

  • Yoshinaga K, Arimura S, Hirata A, Niwa Y, Yun D-J, Tsutsumi N, Uchimiya H, Kawai-Yamada M (2005) Mammalian Bax initiates plant cell death through organelle destruction. Plant Cell Rep 24:408–417

    Article  PubMed  CAS  Google Scholar 

  • Young MJ, Bay D, Hauser G, Court DA (2007) The evolutionary history of mitochondrial porins. BMC Evol Biol 7:31–52

    Article  PubMed  Google Scholar 

  • Yu XH, Perdue TD, Heimer YM, Jones AM (2002) Mitochondrial involvement in tracheary element programmed cell death. Cell Death Differ 9:189–198

    Article  PubMed  CAS  Google Scholar 

  • Yuan S, Fu Y, Wang X, Shi H, Huang Y, Song X, Li L, Song N, Luo Y (2008) Voltage-dependent anion channel 1 is involved in endostatin-induced endothelial cell apoptosis. FASEB J 22:2809–2820

    Article  PubMed  CAS  Google Scholar 

  • Zalman LS, Nikaido H, Kagawa Y (1980) Mitochondrial outer membrane contains a protein producing nonspecific diffusion channels. J Biol Chem 255:1771–1774

    PubMed  CAS  Google Scholar 

  • Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Petit PX, Mignotte B, Kroemer G (1995) Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182:367–377

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We apologize to the researchers whose studies are not cited in this review due to space limitation. We profusely thank Dr. Prakash Kumar for the invitation to write this review article. Comments and suggestions on the manuscript from the editor and two anonymous reviewers are gratefully acknowledged. This study was supported in part by Grant-in-Aids from the Japan Society for the Promotion of Science to TK (19658039 and 21380063) and to YT (21780087), the Saito Gratitude Foundation to CT and the Sumitomo Foundation to YT, and Grant-in-Aid for Scientific Research for Plant Graduate Student from the Nara Institute of Science and Technology (supported by the Ministry of Education, Culture, Sports, Science, and Technology of Japan) to CT. CT is a recipient of the research fellowship for young scientists from JSPS. We also thank Dr. Matthew R. Shenton for critically reading the manuscript.

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Authors and Affiliations

  1. Laboratory of Plant Molecular and Cellular Biology, Graduate School of Life Sciences, Tohoku University, 2-1-1 Katahira, Aoba, Sendai-City, Miyagi, 980-8577, Japan

    Tomonobu Kusano, Chika Tateda & Yoshihiro Takahashi

  2. Biodiversity and Climate Research Center, Frankfurt, Germany

    Thomas Berberich

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  1. Tomonobu Kusano
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  2. Chika Tateda
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  3. Thomas Berberich
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  4. Yoshihiro Takahashi
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Correspondence to Tomonobu Kusano.

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Communicated by R. Reski.

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Kusano, T., Tateda, C., Berberich, T. et al. Voltage-dependent anion channels: their roles in plant defense and cell death. Plant Cell Rep 28, 1301–1308 (2009). https://doi.org/10.1007/s00299-009-0741-z

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