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Mitochondrion and Chloroplast Regulation of Plant Programmed Cell Death

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Book cover Plant Programmed Cell Death

Abstract

Programmed cell death (PCD) is a fundamental process that occurs in plants during development, the hypersensitive response and situations involving abiotic or biotic stress. One form of PCD is characterised morphologically by the retraction of the protoplast from the cell wall and has been observed in many examples of the aforementioned processes. The mitochondria play a significant role in plant PCD, and research has begun to provide us with answers about the role of the chloroplast in plant PCD. In this chapter we discuss what happens when the mitochondria and chloroplast sense and respond to stress or developmental signals and whether they can play a coordinated role in determining whether a plant cell will live or die.

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References

  1. Lockshin RA, Zakeri Z (2004) Apoptosis, autophagy, and more. Int J Biochem Cell Biol 36:2405–2419

    Article  CAS  PubMed  Google Scholar 

  2. Kacprzyk J, Daly CT, McCabe PF (2011) The botanical dance of death: programmed cell death in plants. In: Kader J-C, Delseny M (eds) Advances in botanical research, vol 60. Academic, Burlington, pp 169–261

    Chapter  Google Scholar 

  3. Williams GT, Smith CA, McCarthy NJ, Grimes EA (1992) Apoptosis: final control point in cell biology. Trends Cell Biol 2:263–267

    Article  CAS  PubMed  Google Scholar 

  4. Reape TJ, McCabe PF (2008) Apoptotic-like programmed cell death in plants. New Phytol 180:13–26

    Article  CAS  PubMed  Google Scholar 

  5. Reape TJ, Molony EM, McCabe PF (2008) Programmed cell death in plants: distinguishing between different modes. J Exp Bot 59:435–444

    Article  CAS  PubMed  Google Scholar 

  6. McCabe PF, Levine A, Meijer PJ, Tapon NA, Pennell RI (1997) A programmed cell death pathway activated in carrot cells cultured at a low density. Plant J 12:267–280

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zuppini A, Bugno V, Baldan B (2006) Monitoring programmed cell death triggered by mild heat shock in soybean-cultured cells. Funct Plant Biol 33:617–627

    Article  CAS  PubMed  Google Scholar 

  10. Hogg B, Kacprzyk J, Molony EM, O’Reilly C, Gallagher TF, Gallois P (2011) An in vivo root hair assay for determining rates of apoptotic-like programmed cell death in plants. Plant Methods 7:45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Dauphinee AN, Warner S, Gunawardena AH (2014) A comparison of induced and developmental cell death morphologies in lace plant (Aponogeton madagascariensis) leaves. BMC Plant Biol 14:389

    Article  PubMed  PubMed Central  Google Scholar 

  12. Levine A, Pennell RI, Alvarez ME, Palmer R, Lamb C (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr Biol 6:427–437

    Article  CAS  PubMed  Google Scholar 

  13. Mittler R, Simon L, Lam E (1997) Pathogen-induced programmed cell death in tobacco. J Cell Sci 110:1333–1344

    Article  CAS  PubMed  Google Scholar 

  14. Curtis MJ, Wolpert TJ (2004) The victorin-induced mitochondrial permeability transition precedes cells shrinkage and biochemical markers of cell death, and shrinkage occurs without loss of membrane integrity. Plant J 38:244–259

    Article  CAS  PubMed  Google Scholar 

  15. Yano A, Suzuki K, Uchimiya H, Shinshi H (1998) Induction of hypersensitive cell death by a fungal protein in cultures of tobacco cells. Mol Plant-Microbe Interact 11:115–123

    Article  CAS  Google Scholar 

  16. Gunawardena AHLAN, Sault K, Donnelly P, Greenwood JS, Dengler NG (2004) Programmed cell death remodels lace plant leaf shape during development. Plant Cell 16:60–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Delorme V, McCabe PF, Kim DJ, Leaver CJ (2002) A matrix metalloproteinase gene is expressed at the boundary of senescence and programmed cell death in cucumber. Plant Physiol 123:917–927

    Article  Google Scholar 

  18. Papini A, Mosti S, Brighigna L (1998) Programmed-cell-death events during tapetum development in angiosperms. Protoplasma 207:213–221

    Article  Google Scholar 

  19. 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  CAS  PubMed  PubMed Central  Google Scholar 

  20. Diamond M, McCabe PF (2011) Mitochondrial regulation of plant programmed cell death. In: Kempken F (ed) Plant mitochondria, vol 1, Advances in plant biology. Springer, New York, pp 439–465

    Chapter  Google Scholar 

  21. Doyle SM, Diamond M, McCabe PF (2010) Chloroplast and reactive oxygen species involvement in apoptotic-like programmed cell death in Arabidopsis suspension cultures. J Exp Bot 61:473–482

    Article  CAS  PubMed  Google Scholar 

  22. Gutiérrez J, González-Pérez S, García-García F, Daly CT, Lorenzo O, Revueita JL et al (2014) Programmed cell death activated by Rose Bengal in Arabidopsis thaliana cell suspension cultures requires functional chloroplasts. J Exp Bot 65:3081–3095

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Desagher S, Martinou J-C (2000) Mitochondria as the central control point of apoptosis. Trends Cell Biol 10:369–377

    Article  CAS  PubMed  Google Scholar 

  24. Wang X (2001) The expanding role of mitochondria in apoptosis. Genes Dev 15:2922–2933

    CAS  PubMed  Google Scholar 

  25. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–1312

    Article  CAS  PubMed  Google Scholar 

  26. Jones A (2000) Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends Plant Sci 5:225–230

    Article  CAS  PubMed  Google Scholar 

  27. Bras M, Queenan B, Susin SA (2005) Programmed cell death via mitochondria: different modes of dying. Biochemistry (Mosc) 70:231–239

    Article  CAS  Google Scholar 

  28. Green D, Kroemer G (1998) The central executioners of apoptosis: caspases or mitochondria? Trends Cell Biol 8:267–271

    Article  CAS  PubMed  Google Scholar 

  29. Saelens X, Festjens N, Vande Walle L, van Gurp M, van Loo G, Vandenabeele P (2004) Toxic proteins released from mitochondria in cell death. Oncogene 23:2861–2874

    Article  CAS  PubMed  Google Scholar 

  30. Cai J, Yang J, Jones DP (1998) Mitochondrial control of apoptosis: the role of cytochrome c. Biochim Biophys Acta 1366:139–149

    Article  CAS  PubMed  Google Scholar 

  31. Du C, Fang M, Li Y, Li L, Wang X (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102:33–42

    Article  CAS  PubMed  Google Scholar 

  32. van Loo G, van Gurp M, Depuydt B, Srinivasula SM, Rodriguez I, Alnemri E et al (2002) The serine protease Omi/HtrA2 is released from mitochondria during apoptosis. Omi interacts with caspase-inhibitor XIAP and induces enhanced caspase activity. Cell Death Differ 9:20–26

    Article  PubMed  Google Scholar 

  33. Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C, Kroemer G (2006) Mechanisms of cytochrome c release from mitochondria. Cell Death Differ 13:1423–1433

    Article  CAS  PubMed  Google Scholar 

  34. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Gonzales DH, Neupert W (1990) Biogenesis of mitochondrial c-type cytochromes. J Bioenerg Biomembr 22:753–768

    CAS  PubMed  Google Scholar 

  36. Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86:147–157

    Article  CAS  PubMed  Google Scholar 

  37. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD et al (1999) Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspase-2, -3, -6, -7, -8, and -10 in a caspase-9 dependent manner. J Cell Biol 144:281–292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Van de Craen M, Declercq W, Van den Brande I, Fiers W, Vandenabeele P (1999) The proteolytic procaspase activation network: an in vitro analysis. Cell Death Differ 6:1117–1124

    Article  PubMed  CAS  Google Scholar 

  39. Schimmer AD (2004) Inhibitor of apoptosis proteins: translating basic knowledge into clinical practice. Cancer Res 64:7183–7190

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  41. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2:183–192

    Article  CAS  PubMed  Google Scholar 

  42. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli KJ et al (1998) Two CD95 (APO-1/Fas) signaling pathways. EMBO J 17:1675–1687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Luo X, Budihardjo I, Zou H, Slaughter C, Wang XD (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94:481–490

    Article  CAS  PubMed  Google Scholar 

  44. 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 

  45. Balk J, Chew SK, Leaver CJ, McCabe PF (2003) The intermembrane space of plant mitochondria contains a DNase activity that may be involved in programmed cell death. Plant J 34:1–11

    Article  Google Scholar 

  46. 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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  49. Vacca RA, Valenti D, Bobba A, Merafina RS, Passarella S, Marra E (2006) Cytochrome c is released in a reactive oxygen species-dependent manner and is degraded via caspase-like proteases in tobacco Bright-Yellow 2 cells en route to heat shock-induced cell death. Plant Physiol 141:208–219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Diamond M, Reape TJ, Rocha O, Doyle SM, Kacprzyk J, Doohan FM, McCabe PF (2013) The fusarium mycotoxin deoxynivalenol can inhibit plant apoptosis-like programmed cell death. PLoS One 8(7):e 69542

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  52. Thomas SG, Frankliln-Tong VE (2004) Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429:305–309

    Article  CAS  PubMed  Google Scholar 

  53. Kiba A, Takata O, Ohnishi K, Hikichi Y (2006) Comparative analysis of induction pattern of programmed cell death and defense related responses during hypersensitive cell death and development of bacterial necrotic leaf spots in eggplant. Planta 224:981–994

    Article  CAS  PubMed  Google Scholar 

  54. Uren AG, O’Rourke K, Aravind I, Pisabarro MT, Sehagiri S, Koonin EV, Dixit VM (2000) Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell 6:961–967

    CAS  PubMed  Google Scholar 

  55. Vartapetian AB, Tuzhikov AI, Chichkova NV, Taliansky M, Wolpert TJ (2011) A plant alternative to animal caspases: subtilisin-like proteases. Cell Death Differ 18:1289–1297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Youle RJ, Strasser A (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9:47–59

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Mitsuhara I, Malik KA, Miura M, Ohashi Y (1999) Animal cell-death suppressors Bcl-x(L) and Ced-9 inhibit cell death in tobacco plants. Curr Biol 15:775–778

    Article  Google Scholar 

  60. Zhang L, Xing D (2008) Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death. Plant Cell Physiol 49:1092–1111

    Article  CAS  PubMed  Google Scholar 

  61. Gao C, Xing D, Li L, Xhang L (2008) Implication of reactive oxygen species and mitochondrial dysfunction in the early stages of plant programmed cell death induced by ultraviolet-C overexposure. Planta 227:755–767

    Article  CAS  PubMed  Google Scholar 

  62. Garcia-Heredia JM, Hervás M, De la Rosa MA, Navarro JA (2008) Acetylsalicylic acid induced programmed cell death in Arabidopsis cell cultures. Planta 228:89–97

    Article  CAS  PubMed  Google Scholar 

  63. Crompton M (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem J 341:233–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  65. Saviani EE, Orsi CH, Oliveira JF, Pinto-Maglio CA, Salgado I (2002) Participation of the mitochondrial permeability transition pore in nitric oxide-induced plant cell death. FEBS Lett 510:136–140

    Article  CAS  PubMed  Google Scholar 

  66. 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  CAS  PubMed  PubMed Central  Google Scholar 

  67. Lord CEN, Wertman JN, Lane S, Gunawardena AH (2011) Do mitochondria play a role in remodelling lace plant leaves during programmed cell death? BMC Plant Biol 11:102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Lord CE, Dauphinee AN, Watts RL, Gunawarden AH (2013) Unveiling interactions among mitochondria, caspase-like proteases, and the actin cytoskeleton during plant programmed cell death (PCD). PLoS One 8(3):e57110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Jiao J, Sun L, Zhou B, Gao Z, Hao Y, Zhu X, Liang Y (2014) Hydrogen peroxide production and mitochondrial dysfunction contribute to the fusaric acid-induced programmed cell death in tobacco cells. J Plant Physiol 171:1197–1203

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Wilson JE (2003) Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J Exp Biol 206:2049–2057

    Article  CAS  PubMed  Google Scholar 

  72. Majewski N, Nogueira V, Bhaskar P, Coy PE, Skeen JE, Gotlob K, Chandel NS, Thompson CB, Brooks Robey R, Hay N (2004) Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol Cell 16:819–830

    Article  CAS  PubMed  Google Scholar 

  73. Camocho-Pereira J, Meyer LE, Machado LB, Oliveira MF, Galina A (2009) Reactive oxygen species production by potato tuber mitochondria is modulated by mitochondrially bound hexokinase activity. Plant Physiol 149:1099–1110

    Article  CAS  Google Scholar 

  74. Godbole A, Dubey AK, Reddy PS, Udayakumar M, Mathew MK (2013) Mitochondrial VDAC and hexokinase together modulate plant programmed cell death. Protoplastoma 250:875–884

    Article  CAS  Google Scholar 

  75. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  76. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological response. Plant Cell 17:1866–1875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. De Pinto MC, Locato V, De Gara L (2012) Redox regulation in plant programmed cell death. Plant Cell Environ 35:234–244

    Article  PubMed  CAS  Google Scholar 

  78. Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35(2):259–270

    Google Scholar 

  79. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28:1091–1101

    Article  CAS  PubMed  Google Scholar 

  80. Mullineaux P, Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5:43–48

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  82. Doyle SM, McCabe PF (2010) Type and cellular localisation of reactive oxygen species determine activation or suppression of programmed cell death in Arabidopsis suspension cultures. Plant Signal Behav 4:467–468

    Article  Google Scholar 

  83. Lu H, Wan Q, Wang H, Na X, Wang Z, Bi Y (2012) Oxidative stress and mitochondrial dysfunctions are early events in narciclasine-induced programmed cell death in tobacco Bright Yellow-2 cells. Physiol Plant 144:48–58

    Article  CAS  PubMed  Google Scholar 

  84. Blackstone NW, Green DR (1999) The evolution of a mechanism of cell suicide. Bioessays 21:84–88

    Article  CAS  PubMed  Google Scholar 

  85. Maxwell DP, Nickels R, McIntosh L (2002) Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J 29:269–279

    Article  CAS  PubMed  Google Scholar 

  86. Jabs T (1999) Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem Pharmacol 57:231–245

    Article  CAS  PubMed  Google Scholar 

  87. Blackstone NW, Kirkwood TBL (2003) Mitochondria and programmed cell death: “slave revolt” or community homeostasis? In: Hammerstein P (ed) Genetic and cultural evolution of cooperation. The MIT Press, Cambridge, MA, pp 309–325

    Google Scholar 

  88. Qi Y, Wang H, Zou Y, Liu C, Liu Y, Wang Y, Zhang W (2011) Over-expression of mitochondrial heat shock protein 70 suppresses programmed cell death in rice. FEBS Lett 585:231–239

    Article  CAS  PubMed  Google Scholar 

  89. Zeier J, Pink B, Mueller MJ, Berger S (2004) Light conditions influence specific defence responses in incompatible plant-pathogen interactions: uncoupling systemic resistance from salicylic acid and PR-1 accumulation. Planta 219:673–683

    Article  CAS  PubMed  Google Scholar 

  90. Chandra-Shekara AC, Gupte M, Navarre D, Raina S, Raina R, Klessig D, Kachroo P (2006) Light-dependent hypersensitive response and resistance signaling against turnip crinkle virus in Arabidopsis. Plant J 45:320–334

    Article  CAS  PubMed  Google Scholar 

  91. Morker KH, Roberts MR (2011) Light exerts multiple levels of influence on the Arabidopsis wound response. Plant Cell Environ 34:717–728

    Article  CAS  PubMed  Google Scholar 

  92. Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7:323–328

    Article  CAS  PubMed  Google Scholar 

  93. Mullineaux PM, Baker NR (2010) Oxidative stress: antagonistic signaling for acclimation or cell death? Plant Physiol 154:521–525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Danon A, Rotari VI, Gordon A, Mailhac N, Gallois P (2004) Ultraviolet-c overexposure induces programmed cell death in Arabidopsis, which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35 and defender against apoptotic death. J Biol Chem 279:779–787

    Article  CAS  PubMed  Google Scholar 

  95. Asai T, Stone JM, Heard JE, Kovtun Y, Yorgey P, Sheen J, Ausubel FM (2000) Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell 12:1823–1835

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Dzyubinskaya EV, Kiselevsky DB, Bakeeva LE, Samuilov VD (2006) Programmed cell death in plants: effects of protein synthesis inhibitors and structural changes in pea guard cells. Biochem (Moscow) 71:395–405

    Article  CAS  Google Scholar 

  97. Genoud T, Buchala AJ, Chua N-H, Métraux J-P (2002) Phytochrome signalling modulates the SA-perceptive pathway in Arabidopsis. Plant J 31:87–95

    Article  CAS  PubMed  Google Scholar 

  98. Seo S, Okamoto M, Iwai T, Iwano M, Fukui K, Isogai A, Nakajima N, Ohashi Y (2000) Reduced levels of chloroplast FtsH protein in tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive reaction. Plant Cell 12:917–932

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Kim C, Meskauskiene R, Zhang S, Lee KP, Lakshmanan Ashok M, Blajecka K et al (2012) Chloroplasts of Arabidopsis are the source and a primary target of a plant-specific programmed cell death signalling pathway. Plant Cell 24:3026–3039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Peters JS, Chin C (2005) Evidence for cytochrome f involvement in eggplant cell death induced by palmitoleic acid. Cell Death Differ 12:405–407

    Article  CAS  PubMed  Google Scholar 

  101. Zuppini A, Gerotto C, Moscatiello R, Bergantino E, Baldan B (2009) Chlorella saccharophila cytochrome f and its involvement in the heat shock response. J Exp Bot 60:4189–4200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Wang H, Zhu X, Li H, Cui J, Liu C, Chen X, Zhang W (2014) Induction of caspase-3-like activity in rice following release of cytochrome-f from the chloroplast and subsequent interaction with the ubiquitin-proteasome system. Sci Rep 4:5989

    Google Scholar 

  103. Logan DC, Leaver CJ (2000) Mitochondria-targeted GFP highlights the heterogeneity of mitochondrial shape, size and movement within living plant cells. Mol Biol 51:865–871

    CAS  Google Scholar 

  104. Yao N, Greenberg JT (2006) Arabidopsis accelerated cell death 2 modulates programmed cell death. Plant Cell 18:397–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Bi YH, Chen WL, Zhang WN, Zhou Q, LiJuan Yun LJ, Xing D (2009) Production of reactive oxygen species, impairment of photosynthetic function and dynamic changes in mitochondria are early events in cadmium-induced cell death in Arabidopsis thaliana. Biol Cell 101:629–643

    Article  CAS  PubMed  Google Scholar 

  106. Wertman J, Lord CEN, Dauphinee AN, Gunawardena AHLAN (2012) The pathway of cell dismantling during programmed cell death in lace plant (Aponogeton madagascariensis) leaves. BMC Plant Biol 12:115

    Article  PubMed  PubMed Central  Google Scholar 

  107. Mach JM, Castillo AR, Hoogstraten R, Greenberg JT (2001) The Arabidopsis-accelerated cell death gene, ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc Natl Acad Sci U S A 98:771–776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Greenberg JT, Guo A, Klessi DF, Ausubel FM (1994) Programmed cell death in plants, a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77:551–563

    Article  CAS  PubMed  Google Scholar 

  109. Pattanayak GK, Venkataramani S, Hortensteiner S, Kunz L, Christ B, Moulin M et al (2012) Accelerated cell death 2 suppresses mitochondrial oxidative bursts and modulates cell death in Arabidopsis. Plant J 69:589–600

    Article  CAS  PubMed  Google Scholar 

  110. Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877

    Article  CAS  PubMed  Google Scholar 

  111. Carrie C, Giraud E, Whelan J (2009) Protein transport in organelles: dual targeting of proteins to mitochondria and chloroplasts. FEBS J 276:1187–1195

    Article  CAS  PubMed  Google Scholar 

  112. Glaser E, Whelan J (2011) Protein import into plant mitochondria. In: Kemken F (ed) Plant mitochondria, vol 1, Advances in plant biology. Springer, New York, pp 261–287

    Chapter  Google Scholar 

  113. Welchen E, García L, Mansilla N, Gonzalez DH (2014) Coordination of plant mitochondrial biogenesis: keeping pace with cellular requirements. Front Plant Sci 4:1–12

    Article  Google Scholar 

  114. Carrie C, Small I (1833) A reevaluation of dual-targeting of proteins to mitochondria and chloroplasts. Biochim Biophys Acta 2013:253–259

    Google Scholar 

  115. Lisenbee CS, Lingard MJ, Trelease RN (2005) Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase. Plant J 43:900–914

    Article  CAS  PubMed  Google Scholar 

  116. Susin SA, Lorenzo HK, Samzami N et al (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441–446

    Article  CAS  PubMed  Google Scholar 

  117. Lipton SA, Bossy-Wetzel E (2002) Dueling activities of AIF in cell death versus survival: DNA binding and redox activity. Cell 111:147–150

    Article  CAS  PubMed  Google Scholar 

  118. Joza N, Pospisilik JA, Hangen E, Hanada T, Modjtahedi N, Penninger JM, Kroemer G (2009) AIF: Not just an apoptosis-inducing factor. Ann N Y Acad Sci 1171:2–11

    Article  CAS  PubMed  Google Scholar 

  119. Yamada T, Ichimura K, Kanekatsu M, van Doorn WG (2009) Homologs of genes associated with programmed cell death in animal cells are differentially expressed during senescence of Ipomoea nil petals. Plant Cell Physiol 50:610–625

    Article  CAS  PubMed  Google Scholar 

  120. Wang C, Youle RJ (2009) The role of mitochondria in apoptosis. Annu Rev Genet 43:95–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Eltayeb AE, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Shibahara T et al (2007) Overexpression of monodehydroascorbate reductase in transgenic tobacco, confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta 225:1255–1264

    Article  CAS  PubMed  Google Scholar 

  122. Eltayeba AE, Kawanob N, Badawi GH, Kaminaka H, Sanekata T, Morishima I et al (2006) Enhanced tolerance to ozone and drought stresses in transgenic tobacco overexpressing dehydroascorbate reductase in cytosol. Physiol Plant 127:57–65

    Article  Google Scholar 

  123. Nishikawa F, Kato M, Hyodo H, Ikoma Y, Suglura M, Yano M (2003) Ascorbate metabolism in harvested broccoli. J Exp Bot 54:2439–2448

    Article  CAS  PubMed  Google Scholar 

  124. Chen S, Dickman MB (2004) Bcl-2 family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides. J Exp Bot 55:2617–2623

    Article  CAS  PubMed  Google Scholar 

  125. Yang Y, Haiyan J, Chen Y, Lin W, Wang C, Chen Z et al (2012) A chloroplast envelope membrane protein containing a putative LrgB domain related to the control of bacterial death and lysis is required for chloroplast development in Arabidopsis thaliana. New Phytol 193:81–95

    Article  CAS  PubMed  Google Scholar 

  126. Wang J, Bayles KW (2013) Programmed cell death in plants: lessons from bacteria? Trends Plant Sci 18:133–139

    Article  CAS  PubMed  Google Scholar 

  127. Pang X, Moussa SH, Targy NM, Bose JL, George NM, Gries C et al (2011) Active Bax and Bak are functional holins. Genes Dev 25:2278–2290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Paul F. McCabe .

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Reape, T.J., Brogan, N.P., McCabe, P.F. (2015). Mitochondrion and Chloroplast Regulation of Plant Programmed Cell Death. In: Gunawardena, A.N., McCabe, P.F. (eds) Plant Programmed Cell Death. Springer, Cham. https://doi.org/10.1007/978-3-319-21033-9_2

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