Abstract
Programmed cell death (PCD) refers to the death of a cell that is genetically programmed. Alongside cell division and cell migration, PCD enables the organism to strictly control cell numbers and tissue size as well as to protect itself from unwanted cells that threaten homeostasis. Programmed cell death, specifically apoptosis, a physiological form of cell death, was first reported in the nematode C. elegans in 1972. Since this initial discovery, the functional roles of programmed cell death have been intensely scrutinized and observed across kingdoms ranging from animals to plants. Akin to their mammalian counterparts studies have shown that PCD pathways are vital players in the mediation of plant responses to a range of abiotic stresses, including drought. This chapter will provide: (1) an overview of PCD and its roles during development and in response to environmental stimuli; (2) comprehensive literature review of PCD with details of execution and regulation of apoptosis—the most understood form of PCD; (3) PCD and factors that induce cell death in plants; (4) physiological basis of manipulation of PCD pathways enhancing tolerance to abiotic stress in plant; (5) molecular studies of manipulation of PCD pathways as a mechanism of drought stress tolerance in plants and (6) implication and future directions.
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References
Acehan D, Jiang X, Morgan DG, Heuser JE, Wang X, Akey CW. Three-dimensional structure of the apoptosome: implications for assembly, Procaspase-9 binding, and activation. Mol Cell. 2002;9:423–32. doi:http://dx.doi.org/10.1016/S1097-2765(02)00442-2.
Algeciras-Schimnich A, Shen L, Barnhart BC, Murmann AE, Burkhardt JK, Peter ME. Molecular ordering of the initial signaling events of CD95. Mol Cell Biol. 2002;22:207–20.
Awada T, Dunigan DD, Dickman MB. Animal anti-apoptotic genes ameliorate the loss of turgor in water-stressed transgenic tobacco. Can J Plant Sci. 2003;83:499–506.
Barry M, Bleackley RC. Cytotoxic T lymphocytes: all roads lead to death. Nat Rev Immunol. 2002;2:401–9.
Beers EP. Programmed cell death during plant growth and development. Cell Death Differ. 1997;4:649–61.
Bergsbaken T, Fink SL, Cookson BT. Pyroptosis: host cell death and inflammation. Nat Rev Micro. 2009;7:99–109.
Bethke P, Lonsdale J, Fath A, Jones R. Hormonally regulated programmed cell death in barley aleurone cells. Plant Cell. 1999;11:1033–46.
Birnbaum MJ, Clem RJ, Miller LK. An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs. J Virol. 1994;68:2521–8.
Blumwald E. Sodium transport and salt tolerance in plants. Curr Opin Cell Biol. 2000;12:431–4. doi:http://dx.doi.org/10.1016/S0955-0674(00)00112-5.
Boatright KM, Salvesen GS. Mechanisms of caspase activation. Curr Opin Cell Biol. 2003;15:725–31. doi:http://dx.doi.org/10.1016/j.ceb.2003.10.009.
Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu J-K. Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell. 2005;123:1279–91. doi:http://dx.doi.org/10.1016/j.cell.2005.11.035.
Bozhkov P, Filonova L, Suarez M. Programmed cell death in plant embryogenesis. Curr Top Dev Biol. 2005;67:135–79.
Bredesen DE. Apoptosis: overview and signal transduction pathways. J Neurotrauma. 2000;17:801–10.
Brenner D, Mak TW. Mitochondrial cell death effectors. Curr Opin Cell Biol. 2009;21:871–7. doi:http://dx.doi.org/10.1016/j.ceb.2009.09.004.
Cain K, Bratton SB, Langlais C, Walker G, Brown DG, Sun X-M, Cohen GM. Apaf-1 oligomerizes into biologically active ∼700-kda and inactive ∼1.4-mda apoptosome complexes. J Biol Chem. 2000;275:6067–70. doi:10.1074/jbc.275.9.6067.
Cecconi F, Alvarez-Bolado G, Meyer BI, Roth KA, Gruss P. Apaf1 (CED-4 Homolog) regulates programmed cell death in mammalian development. Cell. 1998;94:727–37. doi:http://dx.doi.org/10.1016/S0092-8674(00)81732-8.
Cha-Um S, Supaibulwattana K, Kirdmanee C. Comparative effects of salt stress and extreme pH stress combined on glycinebetaine accumulation, photosynthetic abilities and growth characters of two rice genotypes. Rice Sci. 2009;16:274–82. doi:10.1016/s1672-6308(08)60091-8.
Chawla S, Jain S, Jain V. Salinity induced oxidative stress and antioxidant system in salt-tolerant and salt-sensitive cultivars of rice (Oryza sativa L.). J Plant Biochem Biotechnol. 2013;22:27–34. doi:10.1007/s13562-012-0107-4.
Chen S, Dickman MB. Bcl-family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides. J Exp Bot. 2004;55:2617–23.
Chen M, Wang J. Initiator caspases in apoptosis signaling pathways. Apoptosis. 2002;7:3139. doi:http://dx.doi.org/10.1023/A:1016167228059.
Chichkova NV, Kim SH, Titova ES, Kalkum M, Morozov VS, Rubtsov YP, Kalinina NO, Taliansky ME, Vartapetian AB. A plant caspase-like protease activated during the hypersensitive response. Plant Cell. 2004;16:157–71. doi:10.1105/tpc.017889.
Chichkova NV, Shaw J, Galiullina RA, Drury GE, Tuzhikov AI, Kim SH, Kalkum M, Hong TB, Gorshkova EN, Torrance L, Vartapetian AB, Taliansky M. Phytaspase, a relocalisable cell death promoting plant protease with caspase specificity. EMBO J. 2010;29:1149–61.
Chinnaiyan AM, Dixit VM. The cell-death machine. Curr Biol. 1996;6:555–62. doi:http://dx.doi.org/10.1016/S0960-9822(02)00541-9.
Chinnaiyan AM, O’Rourke K, Tewari M, Dixit VM. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell. 1995;81:505–12. doi:http://dx.doi.org/10.1016/0092-8674(95)90071-3.
Clem RJ, Miller LK. Control of programmed cell death by the baculovirus genes p35 and IAP. Mol Cell Biol. 1994;14:5212–22.
Coffeen WC, Wolpert TJ. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell. 2004;16:857–73.
Collazo C, Chacón O, Borrás O. Programmed cell death in plants resembles apoptosis of animals. Biotecnol Apl. 2006;23:1–10.
Cominelli E, Conti L, Tonelli C, Galbiati M. Challenges and perspectives to improve crop drought and salinity tolerance. New Biotechnol. 2013;30:355–61. doi:http://dx.doi.org/10.1016/j.nbt.2012.11.001.
Cramer GR, Läuchli A, Polito VS. Displacement of Ca2+ by Na+ from the plasmalemma of root cells: a primary response to salt stress? Plant Physiol. 1985;79:207–11.
Crook NE, Clem RJ, Miller LK. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J Virol. 1993;67:2168–74.
Dangl JL, Jones JDG. Plant pathogens and integrated defence responses to infection. Nature. 2001;411:826–33. doi:http://dx.doi.org/10.1038/35081161.
Danial NN. BCL-2 family proteins: Critical checkpoints of apoptotic cell death. Clin Cancer Res. 2007;13:7254–63. doi:10.1158/1078-0432.ccr-07-1598.
Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell. 2004;116:205–19. doi:http://dx.doi.org/10.1016/S0092-8674(04)00046-7.
Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F. Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci. 2000;57:779–95. doi:10.1007/s000180050041.
Dellaporta SL, Calderon-Urrea A. The sex determination process in maize. Science. 1994;266:1501–5. doi:10.2307/2885174.
Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, Sokolik A, Yurin V. Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci. 2010;123:1468–79. doi:10.1242/jcs.064352.
Deveraux QL, Reed JC. IAP family proteins—suppressors of apoptosis. Genes Dev. 1999;13:239–52.
Deveraux QL, Takahashi R, Salvesen GS, Reed JC. X-linked IAP is a direct inhibitor of cell-death proteases. Nature. 1997;388:300–4. doi:10.1038/40901.
Dickman MB, Park YK, Oltersdorf T, Li W, Clemente T, French R. Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci U S A. 2001a;98:6957–62. doi:10.1073/pnas.091108998.
Dickman MB, Park YK, Oltersdorf T, Li W, Clemente T, French R. Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci U S A. 2001b;98:6957–62.
Dionisio-Sese ML, Tobita S. Effects of salinity on sodium content and photosynthetic responses of rice seedlings differing in salt tolerance. J Plant Physiol. 2000;157:54–8. doi:http://dx.doi.org/10.1016/S0176-1617(00)80135-2.
Domínguez F, Cejudo FJ. A comparison between nuclear dismantling during plant and animal programmed cell death. Plant Sci. 2012;197:114–21. doi:10.1016/j.plantsci.2012.09.009.
Doukhanina EV, Chen S, Van Der Zalm E, Godzik A, Reed J, Dickman MB. Identification and functional characterization of the BAG protein family in Arabidopsis thaliana. J Biol Chem. 2006;281:18793–801.
Drew MC, He C-J, Morgan PW. Programmed cell death and aerenchyma formation in roots. Trends Plant Sci. 2000;5:123–7. doi:http://dx.doi.org/10.1016/S1360-1385(00)01570-3.
Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 2000;102:33–42. doi:http://dx.doi.org/10.1016/S0092-8674(00)00008-8.
Eckardt NA. The future of science: food and water for life. Plant Cell. 2009;21:368–72.
Edwards MJ. Apoptosis, the heat shock response, hyperthermia, birth defects, disease and cancer. Where are the common links? Cell Stress Chaperones. 1998;3:213–20.
Ellis HM, Horvitz HR. Genetic control of programmed cell death in the nematode C. elegans. Cell. 1986;44:817–29. doi:http://dx.doi.org/10.1016/0092-8674(86)90004-8.
Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007;35:495–516. doi:10.1080/01926230701320337.
FAO. Declaration of the world summit on food security. 16–18 November 2009, Rome. http://www.fao.org/wsfs/world-summit/wsfs-challenges/en/
FAO. World water day 2012 celebration. UN Conference Centre, Bangkok, 22 March 2012. http://www.fao.org/asiapacific/rap/home/meetings/list/detail/en/?meetings_id=637&year=2012
Fath A, Bethke P, Lonsdale J, Meza-Romero R, Jones R. Programmed cell death in cereal aleurone. Plant Mol Biol. 2000;44:255–66. doi:10.1023/A:1026584207243.
Fath A, Bethke P, Beligni V, Jones R. Active oxygen and cell death in cereal aleurone cells. J Exp Bot. 2002;53:1273–82. doi:10.1093/jexbot/53.372.1273.
Fomicheva AS, Tuzhikov AI, Beloshistov RE, Trusova SV, Galiullina RA, Mochalova LV, Chichkova NV, Vartapetian AB. Programmed cell death in plants. Biochemistry (Mosc). 2012;77:1452–64. doi:10.1134/S0006297912130044.
Foyer CH, Noctor G. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell Online. 2005;17:1866–75. doi:10.1105/tpc.105.033589.
Foyer CH, Shigeoka S. Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol. 2011;155:93–100. doi:10.1104/pp.110.166181.
Fuchs Y, Steller H. Programmed cell death in animal development and disease. Cell. 2011;147:742–58. doi:http://dx.doi.org/10.1016/j.cell.2011.10.033.
Fukuda H, Watanabe Y, Kuriyama H, Aoyagi S, Sugiyama M, Yamamoto R, Demura T, Minami A. Programming of cell death during xylogenesis. J Plant Res. 1998;111:253–6. doi:10.1007/BF02512179.
Fulda S, Gorman AM, Hori O, Samali A. Cellular stress responses: cell survival and cell death. Int J Cell Biol. 2010;2010:23.
García-Sáez AJ. The secrets of the Bcl-2 family. Cell Death Differ. 2012;19:1733–40.
Gewies A. Introduction to apoptosis. ApoReview. 2003;1–26.
Ghosh N, Adak MK, Ghosh PD, Gupta S, Sen Gupta DN, Mandal C. Differential responses of two rice varieties to salt stress. Plant Biotechnology Reports 2011;5:89–103.
Gilchrist DG. Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu Rev Phytopathol. 1998;36:393–414.
Giuliani C, Consonni G, Gavazzi G, Colombo M, Dolfini S. Programmed cell death during embryogenesis in maize. Ann Bot. 2002;90:287–92. doi:10.1093/aob/mcf173.
Goldstein JC, Waterhouse NJ, Juin P, Evan GI, Green DR. The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat Cell Biol. 2000;2:156–62.
Goyal L, Mccall K, Agapite J, Hartwieg E, Steller H. Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J. 2000;19:589–97.
Greenberg JT. Programmed cell death: a way of life for plants. Proc Natl Acad Sci U S A. 1996;93:12094–7.
Groover A, Jones AM. Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol. 1999;119:375–84. doi:10.2307/4278635.
Gunawardena AH, Greenwood JS, Dengler NG. Programmed cell death remodels lace plant leaf shape during development. Plant Cell. 2004;16:60–73.
Gupta S. Molecular steps of death receptor and mitochondrial pathways of apoptosis. Life Sci. 2001;69:2957–64. doi:http://dx.doi.org/10.1016/S0024-3205(01)01404-7.
Hara-Nishimura I, Inoue K, Nishimura M. A unique vacuolar processing enzyme responsible for conversion of several proprotein precursors into the mature forms. FEBS Lett. 1991;294:89–93. doi:http://dx.doi.org/10.1016/0014-5793(91)81349-D.
Hartl FU, Bracher A, Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature. 2011;475:324–32.
Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, et al. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science. 2004;305:855–8.
Hatsugai N, Kuroyanagi M, Nishimura M, Hara-Nishimura I. A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis. 2006;11:905–11. doi:http://dx.doi.org/10.1007/s10495-006-6601-1.
Hay BA, Wassarman DA, Rubin GM. Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell. 1995;83:1253–62. doi:http://dx.doi.org/10.1016/0092-8674(95)90150-7.
Heiden MGV, Chandel NS, Schumacker PT, Thompson CB. Bcl-xL prevents cell death following growth factor withdrawal by facilitating mitochondrial ATP/ADP exchange. Mol Cell. 1999;3:159–67. doi:http://dx.doi.org/10.1016/S1097-2765(00)80307-X.
Hengartner MO. The biochemistry of apoptosis. Nature. 2000;407:770–6. doi:http://dx.doi.org/10.1038/35037710.
Hill RD, Huang S, Stasolla C. Hemoglobins, programmed cell death and somatic embryogenesis. Plant Sci. 2013;211:35–41. doi:http://dx.doi.org/10.1016/j.plantsci.2013.06.010.
Hoang TML. Engineering salinity tolerance in rice by manipulation of exogenous expression of cell death regulators. Ph.D. Thesis. Brisbane: Queensland University of Technology; 2014.
Hoang TML, Williams B, Khanna H, Dale J, Mundree SG. Physiological basis of salt stress tolerance in rice expressing the antiapoptotic gene SfIAP. Funct Plant Biol. 2014;41:1168–77. doi:http://dx.doi.org/10.1071/FP13308.
Hoang TML, Moghaddam L, Williams B, Khanna H, Dale J, Mundree SG. Development of salinity tolerance in rice by constitutive-overexpression of genes involved in the regulation of programmed cell death. Front Plant Sci. 2015;6:175. doi:10.3389/fpls.2015.00175.
Horvitz HR, Ellis HM, Sternberg PW. Programmed cell death in nematode development. Neurosci Comment. 1982;1:56–65.
Hu Y, Benedict MA, Ding L, Núñez G. Role of cytochrome c and dATP/ATP hydrolysis in Apaf-1 mediated caspase-9 activation and apoptosis. EMBO J. 1999;18:3586–95.
Huang Q, Deveraux QL, Maeda S, Salvesen GS, Stennicke HR, Hammock BD, Reed JC. Evolutionary conservation of apoptosis mechanisms: lepidopteran and baculoviral inhibitor of apoptosis proteins are inhibitors of mammalian caspase-9. Proc Natl Acad Sci U S A. 2000;97:1427–32.
Hughes FM Jr., Cidlowski JA. Potassium is a critical regulator of apoptotic enzymes in vitro and in vivo. Adv Enzyme Regul. 1999;39:157–71. doi:http://dx.doi.org/10.1016/S0065-2571(98)00010-7.
Huh G-H, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML, Bressan RA, Hasegawa PM. Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J. 2002;29:649–59. doi:10.1046/j.0960-7412.2001.01247.x.
Ismail A, Heuer S, Thomson M, Wissuwa M. Genetic and genomic approaches to develop rice germplasm for problem soils. Plant Mol Biol. 2007;65:547–70. doi:10.1007/s11103-007-9215-2.
Jiang A-L, Cheng Y, Li J, Zhang W. A zinc-dependent nuclear endonuclease is responsible for DNA laddering during salt-induced programmed cell death in root tip cells of rice. J Plant Physiol. 2008;165:1134–41. doi:10.1016/j.jplph.2007.12.008.
Kabbage M, Dickman MB. The BAG proteins: a ubiquitous family of chaperone regulators. Cell Mol Life Sci. 2008;65:1390–402.
Kabbage M, Li W, Chen S, Dickman MB. The E3 ubiquitin ligase activity of an insect anti-apoptotic gene (SfIAP) is required for plant stress tolerance. Physiol Mol Plant Pathol. 2010;74:351–62. doi:http://dx.doi.org/10.1016/j.pmpp.2010.06.002.
Kader MA, Lindberg S. Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signal Behav. 2010;5:233–8.
Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26:239–57.
King KL, Cidlowski JA. Cell cycle regulation and apoptosis. Annu Rev Physiol. 1998;60:601–17.
Kondo S. Altruistic cell suicide in relation to radiation hormesis. Int J Radiat Biol. 1988;53:95–102. doi:10.1080/09553008814550461.
Kourtis N, Tavernarakis N. Autophagy and cell death in model organisms. Cell Death Differ. 2009;16:21.
Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, Hengartner M, Knight RA, Kumar S, Lipton SA, Malorni W, Nuñez G, Peter ME, Tschopp J, Yuan J, Piacentini M, Zhivotovsky B, Melino G. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009;16:3–11. doi:http://dx.doi.org/10.1038/cdd.2008.150.
Kuo A, Cappelluti S, Cervantes-Cervantes M, Rodriguez M, Bush DS. Okadaic acid, a protein phosphatase inhibitor, blocks calcium changes, gene expression, and cell death induced by gibberellin in wheat aleurone cells. Plant Cell. 1996;8:259–69.
Lam E. Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol. 2004;5:305–15.
Lam E, Kato N, Lawton M. Programmed cell death, mitochondria and the plant hypersensitive response. Nature. 2001;411:848–53.
Leijon K, Hammarström B, Holmberg D. Non-obese diabetic (NOD) mice display enhanced immune responses and prolonged survival of lymphoid cells. Int Immunol. 1994;6:339–45. doi:10.1093/intimm/6.2.339.
Levine A, Tenhaken R, Dixon R, Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994;79:583–93. doi:http://dx.doi.org/10.1016/0092-8674(94)90544-4.
Li W, Dickman M. Abiotic stress induces apoptotic-like features in tobacco that is inhibited by expression of human Bcl-2. Biotechnol Lett. 2004a;26:87–95. doi:10.1023/B:BILE.0000012896.76432.ba.
Li W, Dickman MB. Abiotic stress induces apoptotic-like features in tobacco that is inhibited by expression of human Bcl-2. Biotechnol Lett. 2004b;26:87–95.
Li H, Zhu H, Xu C-J, Yuan J. Cleavage of BID by Caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 1998;94:491–501. doi:http://dx.doi.org/10.1016/S0092-8674(00)81590-1.
Li J-Y, Jiang A-L, Zhang W. Salt stress-induced programmed cell death in rice root tip cells. J Integr Plant Biol. 2007;49:481–6. doi:10.1111/j.1744-7909.2007.00445.x.
Li W, Kabbage M, Dickman MB. Transgenic expression of an insect inhibitor of apoptosis gene, SfIAP, confers abiotic and biotic stress tolerance and delays tomato fruit ripening. Physiol Mol Plant Pathol. 2010;74:363–75. doi:10.1016/j.pmpp.2010.06.001.
Lincoln JE, Craig R, Overduin B, Smith K, Bostock R, Gilchrist DG. Expression of the antiapoptotic baculovirus p35 gene in tomato blocks programmed cell death and provides broad-spectrum resistance to disease. Proc Natl Acad Sci U S A. 2002;99:15217–21.
Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 1996;86:147–57. doi:http://dx.doi.org/10.1016/S0092-8674(00)80085-9.
Liu S-H, Fu B-Y, Xu H-X, Zhu L-H, Zhai H-Q, Li Z-K. Cell death in response to osmotic and salt stresses in two rice (Oryza sativa L.) ecotypes. Plant Sci. 2007;172:897–902. doi:10.1016/j.plantsci.2006.12.017.
Los M, Wesselborg S, Schulze-Osthoff K. The role of caspases in development, immunity, and apoptotic signal transduction: lessons from knockout mice. Immunity. 1999;10:629–39. doi:http://dx.doi.org/10.1016/S1074-7613(00)80062-X.
Lukiw WJ, Bazan NG. Inflammatory, apoptotic, and survival gene signaling in Alzheimer’s disease. A review on the bioactivity of Neuroprotectin D1 and apoptosis. Mol Neurobiol. 2010;42:10–6.
Luthi A, Martin S. The CASBAH: a searchable database of caspase substrates. Cell Death Differ. 2007;14:641–50.
Maathuis FJM, Amtmann A. K+ nutrition and Na+ toxicity: the basis of cellular K+ Na+ ratios. Ann Bot. 1999;84:123–33. doi:http://dx.doi.org/10.1006/anbo.1999.0912.
Marschner P. Marschner’s mineral nutrition of higher plants. Amsterdam: Elsevier Science; 2011.
Martinou J-C, Youle RJ. Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev Cell. 2011;21:92–101.
Miller G, Shulaev V, Mittler R. Reactive oxygen signaling and abiotic stress. Physiol Plant. 2008;133:481–9. doi:10.1111/j.1399-3054.2008.01090.x.
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 2010;33:453–67. doi:10.1111/j.1365-3040.2009.02041.x.
Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002;7:405–10.
Mittler R, Lam E. Sacrifice in the face of foes: pathogen-induced programmed cell death in plants. Trends Microbiol. 1996;4:10–5. doi:http://dx.doi.org/10.1016/0966-842X(96)81499-5.
Munns R. Comparative physiology of salt and water stress. Plant Cell Environ. 2002;25:239–50.
Munns R. Plant adaptations to salt and water stress: differences and commonalities. In: Ismail T, editor. Advances in botanical research. Waltham: Academic Press; 2011. p. 1–32.
Munns R, Tester M. Mechanisms of salinity tolerance. Annu Rev Plant Biol. 2008;59:651–81.
Munns R, James RA, Läuchli A. Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot. 2006;57:1025–43.
Nawkar GM, Maibam P, Park JH, Sahi VP, Lee SY, Kang CH. UV-induced cell death in plants. Int J Mol Sci. 2013;14:1608–28. doi:http://dx.doi.org/10.3390/ijms14011608
Paul J-Y. The manipulation of apoptosis-related genes to generate resistance to fusarium wilt and water stress in banana. Ph.D. Thesis. Brisbane: Queensland University of Technology; 2009.
Paul J-Y, Becker DK, Dickman MB, Harding RM, Khanna HK, Dale JL. Apoptosis-related genes confer resistance to Fusarium wilt in transgenic ‘Lady Finger’ bananas. Plant Biotechnol J. 2011;9:1141–8. doi:10.1111/j.1467-7652.2011.00639.x.
Pennell RI, Lamb C. Programmed cell death in plants. Plant Cell. 1997;9:1157–68.
Pop C, Timmer J, Sperandio S, Salvesen GS. The apoptosome activates Caspase-9 by dimerization. Mol Cell. 2006;22:269–75. doi:http://dx.doi.org/10.1016/j.molcel.2006.03.009.
Portt L, Norman G, Clapp C, Greenwood M, Greenwood MT. Anti-apoptosis and cell survival: a review. Biochim Biophys Acta. 2011;1813, 238-259. doi:http://dx.doi.org/10.1016/j.bbamcr.2010.10.010.
Purring-Koch C, Mclendon G. Cytochrome c binding to Apaf-1: the effects of dATP and ionic strength. Proc Natl Acad Sci. 2000;97:11928–31. doi:10.1073/pnas.220416197.
Qiao J, Mitsuhara I, Yazaki Y, Sakano K, Gotoh Y, Miura M, Ohashi Y. Enhanced resistance to salt, cold and wound stresses by overproduction of animal cell death suppressors Bcl-xl and Ced-9 in tobacco cells—their possible contribution through improved function of organella. Plant Cell Physiol. 2002;43:992–1005.
Raff MC. Social controls on cell survival and cell death. Nature. 1992;356:397–400.
Rami A, Bechmann I, Stehle JH. Exploiting endogenous anti-apoptotic proteins for novel therapeutic strategies in cerebral ischemia. Prog Neurobiol. 2008;85:273–96. doi:http://dx.doi.org/10.1016/j.pneurobio.2008.04.003.
Reape T, Mccabe P. Apoptotic-like regulation of programmed cell death in plants. Apoptosis. 2010;15:249–56. doi:10.1007/s10495-009-0447-2.
Reape TJ, Molony EM, Mccabe PF. Programmed cell death in plants: distinguishing between different modes. J Exp Bot. 2008;59:435–44. doi:10.1093/jxb/erm258.
Renehan AG, Booth C, Potten CS. What is apoptosis, and why is it important? Br Med J. 2001;322:1536–8.
Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN. Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol. 2006;141:357–66. doi:10.1104/pp.106.079129.
Roos WP, Kaina B. DNA damage-induced cell death by apoptosis. Trends Mol Med. 2006;12:440–50. doi:http://dx.doi.org/10.1016/j.molmed.2006.07.007.
Rothe M, Pan M-G, Henzel WJ, Ayres TM, Goeddel DV. The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell. 1995;83:1243–52.
Roy N, Mahadevan MS, Mclean M, Shutter G, Yaraghi Z, Farahani R, Baird S, Besner-Johnston A, Lefebvre C, Kang X, Salih M, Aubry H, Tamai K, Guan X, Ioannou P, Crawford TO, De Jong PJ, Surh L, Ikeda J-E, Korneluk RG, Mackenzie A. The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell. 1995;80:167–78. doi:http://dx.doi.org/10.1016/0092-8674(95)90461-1.
Rudin CM, Thompson CB. Apoptosis and disease: regulation and clinical relevance of programmed cell death. Annu Rev Med. 1997;48:267–81. doi:10.1146/annurev.med.48.1.267.
Russell JH, Ley TJ. Lymphocyte-mediated cytotoxicity. Annu Rev Immunol. 2002;20:323–70. doi:http://search.proquest.com/docview/201638982?accountid=13380.
Sah NK, Taneja TK, Pathak N, Begum R, Athar M, Hasnain SE. The baculovirus antiapoptotic p35 gene also functions via an oxidant-dependent pathway. Proc Natl Acad Sci U S A. 1999;96:4838–43.
Sakahira H, Enari M, Nagata S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature. 1998;391:96–9. doi:http://dx.doi.org/10.1038/34214.
Schimmer AD. Inhibitor of apoptosis proteins: translating basic knowledge into clinical practice. Cancer Res. 2004;64:7183–90. doi:10.1158/0008-5472.can-04-1918.
Shabala S. Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J Exp Bot. 2009;60:709–12. doi:10.1093/jxb/erp013.
Shabala S, Cuin TA. Potassium transport and plant salt tolerance. Physiol Plant. 2008;133:651–69. doi:10.1111/j.1399-3054.2007.01008.x.
Shabala S, Cuin TA, Prismall L, Nemchinov LG. Expression of animal CED-9 anti-apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress. Planta. 2007;227:189–97. doi:10.1007/s00425-007-0606-z.
Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. 2012;2012:26. doi:10.1155/2012/217037.
Shi Y. Caspase activation: revisiting the induced proximity model. Cell. 2004;117:855–8. doi:http://dx.doi.org/10.1016/j.cell.2004.06.007.
Shi Y. Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell. 2002;9:459–70. doi:http://dx.doi.org/10.1016/S1097-2765(02)00482-3.
Simeonova E, Sikora A, Charzyńska M, Mostowska A. Aspects of programmed cell death during leaf senescence of mono- and dicotyledonous plants. Protoplasma. 2000;214:93–101. doi:10.1007/BF02524266.
Smalle J, Vierstra RD. The ubiquitin 26s proteasome proteolytic pathway. Annu Rev Plant Biol. 2004;55:555–90.
Sondermann H, Scheufler C, Schneider C, Hohfeld J, Hartl FU, Moarefi I. Structure of a Bag/Hsc70 complex: convergent functional evolution of Hsp70 nucleotide exchange factors. Science. 2001;291:1553–7.
Soriano ME, Scorrano L. The interplay between BCL-2 family proteins and mitochondrial morphology in the regulation of apoptosis. In: Hetz C, editor. BCL-2 protein family. New York: Springer; 2010. p. 97–114.
Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Alnemri ES. Autoactivation of Procaspase-9 by Apaf-1-mediated oligomerization. Mol Cell. 1998;1:949–57. doi:http://dx.doi.org/10.1016/S1097-2765(00)80095-7.
Strasser A, O’Connor L, Dixit VM. Apoptosis signaling. Annu Rev Biochem. 2000;69:217–45.
Straszewski-Chavez SL, Abrahams VM, Funai EF, Mor G. X-linked inhibitor of apoptosis (XIAP) confers human trophoblast cell resistance to Fas-mediated apoptosis. Mol Hum Reprod. 2004;10:33–41. doi:10.1093/molehr/gah001.
Suarez MF, Filonova LH, Smertenko A, Savenkov EI, Clapham DH, Von Arnold S, Zhivotovsky B, Bozhkov PV. Metacaspase-dependent programmed cell death is essential for plant embryogenesis. Curr Biol. 2004;14:R339–40. doi:http://dx.doi.org/10.1016/j.cub.2004.04.019.
Sussman M. Molecular analysis of protein in the plant plasma membrane. Annu Rev Plant Physiol Plant Mol Biol. 1994;45:211–34.
Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell. 2001;8:613–21. doi:http://dx.doi.org/10.1016/S1097-2765(01)00341-0.
Takayama S, Reed JC. Molecular chaperone targeting and regulation by BAG family proteins. Nat Cell Biol. 2001;3:E237–41.
Timperio AM, Egidi MG, Zolla L. Proteomics applied on plant abiotic stresses: Role of heat shock proteins (HSP). J Proteom. 2008;71:391–411. doi:http://dx.doi.org/10.1016/j.jprot.2008.07.005.
Uren AG, O’Rourke K, Aravind L, Pisabarro MT, Seshagiri S, Koonin EV, Dixit VM. Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell. 2000;6:961–7.
Van Doorn WG. Classes of programmed cell death in plants, compared to those in animals. J Exp Bot. 2011;62:4749–61. doi:10.1093/jxb/err196.
Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol. 2010;11:700–14. doi:http://dx.doi.org/10.1038/nrm2970.
Vartapetian AB, Tuzhikov AI, Chichkova NV, Taliansky M, Wolpert TJ. A plant alternative to animal caspases: subtilisin-like proteases. Cell Death Differ. 2011;18:1289–97.
Vaux DL, Korsmeyer SJ. Cell death in development. Cell. 1999;96:245–54. doi:http://dx.doi.org/10.1016/S0092-8674(00)80564-4.
Vaux DL, Silke J. IAPs, RINGs and ubiquitylation. Nat Rev Mol Cell Biol. 2005;6:287–97. doi:http://dx.doi.org/10.1038/nrm1621.
Vaux DL, Strasser A. The molecular biology of apoptosis. Proc Natl Acad Sci U S A. 1996;93:2239–44.
Vaux DL, Cory S, Adams JM. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature. 1988;335:440–2.
Vaux DL, Haecker G, Strasser A. An evolutionary perspective on apoptosis. Cell. 1994;76:777–9. doi:http://dx.doi.org/10.1016/0092-8674(94)90350-6.
Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, Moritz RL, Simpson RJ, Vaux DL. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell. 2000;102:43–53. doi:http://dx.doi.org/10.1016/S0092-8674(00)00009-X.
Wang H, Li J, Bostock R, Gilchrist D. Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell. 1996a;8:375–91.
Wang M, Oppedijk B, Lu X, Duijn B, Schilperoort R. Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Mol Biol. 1996b;32:1125–34. doi:10.1007/BF00041396.
Wang W, Pan J, Zheng K, Chen H, Shao H, Guo Y, Hongwu B, Han N, Wang J, Zhu M. Ced-9 inhibits Al-induced programmed cell death and promotes Al tolerance in tobacco. Biochem Biophys Res Commun. 2009a;383:141–5.
Wang Z, Song J, Zhang Y, Yang B, Chen S. Expression of baculovirus anti-apoptotic p35 gene in tobacco enhances tolerance to abiotic stress. Biotechnol Lett. 2009b;31:585–9.
Wang M, Zheng Q, Shen Q, Guo S. The critical role of potassium in plant stress response. Int J Mol Sci. 2013;14:7370–90.
Whelan RS, Kaplinskiy V, Kitsis RN. Cell death in the pathogenesis of heart disease: mechanisms and significance. Annu Rev Physiol. 2010;72:19–44. doi:10.1146/annurev.physiol.010908.163111.
Williams B, Dickman M. Plant programmed cell death: can’t live with it; can’t live without it. Mol Plant Pathol. 2008;9:531–44.
Williams B, Kabbage M, Britt R, Dickman MB. AtBAG7, an Arabidopsis Bcl-2–associated athanogene, resides in the endoplasmic reticulum and is involved in the unfolded protein response. Proc Natl Acad Sci U S A. 2010;107:6088–93.
Xu P, Rogers SJ, Roossinck MJ. Expression of antiapoptotic genes bcl-xL and ced-9 in tomato enhances tolerance to viral-induced necrosis and abiotic stress. Proc Natl Acad Sci U S A. 2004;101:15805–10.
Xu Z, Zhou G, Shimizu H. Plant responses to drought and rewatering. Plant Signal Behav. 2010;5:649–54.
Yang X, Chang HY, Baltimore D. Autoproteolytic activation of pro-caspases by oligomerization. Mol Cell. 1998;1:319–25. doi:http://dx.doi.org/10.1016/S1097-2765(00)80032-5.
Yen C-H, Yang C-H. Evidence for programmed cell death during leaf senescence in plants. Plant Cell Physiol. 1998;39:922–7.
Yin Q, Park HH, Chung JY, Lin S-C, Lo Y-C, Da Graca LS, Jiang X, Wu H. Caspase-9 Holoenzyme is a specific and optimal Procaspase-3 processing machine. Mol Cell. 2006;22:259–68. doi:http://dx.doi.org/10.1016/j.molcel.2006.03.030.
Yoshida S. Molecular regulation of leaf senescence. Curr Opin Plant Biol. 2003;6:79–84. doi:http://dx.doi.org/10.1016/S1369526602000092.
Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol. 2008;9:47–59. doi:http://dx.doi.org/10.1038/nrm2308.
Young TE, Gallie DR. Programmed cell death during endosperm development. Plant Mol Biol. 2000;44:283–301. doi:http://dx.doi.org/10.1023/A:1026588408152.
Zheng L, Trageser CL, Willerford DM, Lenardo MJ. T cell growth cytokines cause the superinduction of molecules mediating antigen-induced T lymphocyte death. J Immunol. 1998;160:763–9.
Zheng TS, Hunot S, Kuida K, Flavell RA. Caspase knockouts: matters of life and death. Cell Death Differ. 1999;6:1043–53.
Zhu JK. Plant salt tolerance. Trends Plant Sci. 2001;6:66–71. doi:http://dx.doi.org/10.1016/S1360-1385(00)01838-0.
Zhu J, Fu X, Koo YD, Zhu JK, Jenney FEJ, Adams MW, Zhu Y, Shi H, Yun DJ, Hasegawa PM, Bressan RA. An enhancer mutant of Arabidopsis salt overly sensitive 3 mediates both ion homeostasis and the oxidative stress response. Mol Cell Biol. 2007;27:5214–24.
Zimmermann KC, Bonzon C, Green DR. The machinery of programmed cell death. Pharmacol Ther. 2001;92:57–70. doi:http://dx.doi.org/10.1016/S0163-7258(01)00159-0.
Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell. 1997;90:405–13. doi:http://dx.doi.org/10.1016/S0092-8674(00)80501-2.
Zuzarte-Luís V, Hurlé JM. Programmed cell death in the developing limb. Int J Dev Biol. 2002;46:871–6.
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The authors thank Australian Government for financial support through Endeavour Postgraduate Awards.
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Hoang, T.M.L., Williams, B., Mundree, S.G. (2016). Manipulation of Programmed Cell Death Pathways Enhances Osmotic Stress Tolerance in Plants: Physiological and Molecular Insights. In: Hossain, M., Wani, S., Bhattacharjee, S., Burritt, D., Tran, LS. (eds) Drought Stress Tolerance in Plants, Vol 1. Springer, Cham. https://doi.org/10.1007/978-3-319-28899-4_19
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