Abstract
Programmed cell death (PCD) is an active process, which occurs during growth, development and in response to various adverse environmental factors. During the course of growth and development, plants are frequently exposed to various stresses such as salinity, temperatures, heavy metals, drought and biotic factors. Plants have also evolved strategies to overcome these adverse conditions. However, when the intensity of these detrimental factors is high, plant cells undergo a process called PCD, as a part of defense mechanism. PCD is a highly regulated process, in which specific targeted cells are damaged to ensure the survival of the organism. Thus, the process facilitates the removal of unwanted and damaged cells, thus maintaining cellular differentiation and tissue homeostasis. PCD also plays an important role in developmental processes, such as differentiation of tracheary elements, formation of glandular trichomes, abscission of floral organs and embryo formation, and hence, it is a vital process for normal growth and development of plants. Stress-induced PCD significantly determines the crop yield and productivity, and hence, it is significant to agriculture. In this chapter, molecular mechanisms involved in PCD related to abiotic stress involving mitochondria and plastid are discussed.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Affenzeller MJ, Darehshouri A, Andosch A, Lu C, Lütz-Meindl U (2009) Salt stress-induced cell death in the unicellular green alga Micrasterias denticulata. J Exp Bot 60:939–954
Ahlfors R, Brosche M, Kangasjarvi J (2009) Ozone and nitric oxide interaction in Arabidopsis thaliana. Plant Signal Behav 4:878–879
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annl Rev Plant Physiol Plant Mol Biol 50:601–639
Asai T, Stone JM, Heard JE, Kovtun Y, Yorgey P, Sheen J, Ausubel MF (2000) Fumonisin B1 induced cell death in Arabidopsis protoplasts signaling pathways. Plant Cell 12:1823–1835
Atkinson JN, Urwin EP (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3544
Babu TS, Akhtar TA, Lampi MA, Tripuranthakam S, Dixon DG, Greenberg BM (2003) Similar stress responses are elicited by copper and ultraviolet radiation in the aquatic plant Lemna gibba: implication of reactive oxygen species as common signals. Plant Cell Physiol 44:1320–1329
Bhattacharjee S (2012) The language of reactive oxygen species signaling in plants. J Bot 6:1–22
Chai T, Zhou J, Liu J, Xing D (2015) LSD1 and HY5 antagonistically regulate red light induced-programmed cell death in Arabidopsis. Front Plant Sci 6:292
Chang H, Lin C, Huang H (2005) Zinc-induced cell death in rice (Oryza sativa L.) roots. Plant Growth Regul 46:261–266
Chen R, Sun S, Wang C, Li Y, Liang Y, An F, Li C, Dong H, Yang X, Zhang J, Zuo J (2009) The Arabidopsis PARAQUAT RESISTANT2 gene encodes an S-nitrosoglutathione reductase that is a key regulator of cell death. Cell Res 19:1377–1387
Chen J, Sonobe K, Ogawa N, Masuda S, Nagatani A, Kobayashi Y, Ohta H (2013) Inhibition of Arabidopsis hypocotyl elongation by jasmonates is enhanced under red light in phytochrome B dependent manner. J Plant Res 126:161–168
Danon A, Gallois P (1998) UV-C radiation induces apoptotic-like changes in Arabidopsis thaliana. FEBS Lett 437:131–136
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
Danon A, Miersch O, Felix G, Camp R, Apel K (2005) Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana. Plant J 41:68–80
Davison PA, Hunter CN, Horton P (2002) Overexpression of β-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418:203–206
De Block M, Verduyn C, De Brouwer D, Cornelissen M (2005) Poly (ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance. Plant J 41:95–106
De Pinto MC, Locato V, De Gara L (2012) Redox regulation in plant programmed cell death. Plant, Cell Environ 35:234–244
Doyle SM, McCabe PF (2010) Type and cellular location of reactive oxygen species determine activation or suppression of programmed cell death in Arabidopsis suspension. Plant Signal Behav 5:467–468
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
Gadjev I, Stone JM, Gechev TS (2008) Programmed cell death in plants: new insights into redox regulation and the role of hydrogen peroxide. Int Rev Cell Mol Biol 270:87–124
Gao C, Xing D, Li L, Zhang 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
Garnier L, Simon-plas F, Thuleau P, Agnel J, Blein J, Ranjeva R, Montillet J (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant, Cell Environ 29:1956–1969
Gechev TS, Breusegem VF, 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
Gielen B, Low M, Deckmyn G, Metzger U, Franck F, Heerdt C, Matyssek R, Valcke R, Ceulemans R (2007) Chronic ozone exposure affects leaf senescence of adult beech trees: a chlorophyll fluorescence approach. J Exp Bot 58:785–795
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
González Besteiro MA, Bartels S, Albert A, Ulm R (2011) Arabidopsis MAP kinase phosphatase 1 and its target MAP kinases 3 and 6 antagonistically determine UV-B stress tolerance, independent of the UVR8 photoreceptor pathway. Plant J 68:727–737
Hamed-laouti IB, Arbelet-bonnin D, De Bont L, Biligui B, Gakière B, Abdelly C, Ben Hamed K (2016) Comparison of NaCl-induced programmed cell death in the obligate halophyte Cakile maritima and the glycophyte Arabidospis thaliana. Plant Sci 247:49–59
He R, Drury GE, Rotari VI, Gordon A, Willer M, Farzaneh T, Woltering EJ, Gallois P (2008) Metacaspase-8 modulates programmed cell death induced by ultraviolet light and H2O2 in Arabidopsis. J Biol Chem 283:774–783
Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052
Huang X, Li Y, Zhang X, Zuo J, Yang S (2010) The Arabidopsis LSD1 gene plays an important role in the regulation of low temperature-dependent cell death. New Phytol 187:301–312
Huh G, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML, Bressan RA, Hasegawa PM (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J 29:649–659
Jabs T, Dietrich RA, Dang JL (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273:1853–1856
Jaspers P, Kangasjarvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Planta 138:405–413
Jin CW, Mao QQ, Luo BF, Lin XY, Du ST (2013) Mutation of mpk6 enhances cadmium tolerance in Arabidopsis plants by alleviating oxidative stress. Plant Soil 371:387–396
Kadono T, Tran D, Errakhi R, Hiramatsu T, Meimoun P, Briand J, Iwaya-inoue M, Kawano T, Bouteau F (2010) Increased anion channel activity is an unavoidable event in Ozone-induced programmed cell death. PLoS ONE 5:e13373
Keunen E, Remans T, Bohler S, Vangronsveld J, Cuypers A (2011) Metal-induced oxidative stress and plant mitochondria. Int J Mol Sci 12:6894–6918
Kim Y, Wang M, Bai Y, Zeng Z, Guo F, Han N, Bian H, Wang J, Pan J, Zhu M (2014) Bcl-2 suppresses activation of VPE s by inhibiting cytosolic Ca2+ level with elevated K+ efflux in NaCl-induced PCD in rice. Plant Physiol Biochem 80:168–175
Koukalová B, Kovafik M, Fajkus J, Sirok J (1997) Chromatin fragmentation associated with apoptotic changes in tobacco cells exposed to cold stress. FEBS Lett 414:289–292
Lee KP, Kim C, Landgraf F, Apel K (2007) EXECUTER1- AND EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Nat Acad Sci U S A 104:10270–10275
Li Z, Xing D (2011) Mechanistic study of mitochondria dependent programmed cell death induced by aluminium phytotoxicity using fluorescence techniques. J Exp Bot 62:331–343
Li J, Jiang A, Chen H, Wang Y, Zhang W (2007) Lanthanum prevents salt stress-induced programmed cell death in rice root tip cells by controlling early induction events. J Integr Plant Biol 49:1024–1031
Li Z, Yue H, Xing D (2012) MAP Kinase 6-mediated activation of vacuolar processing enzyme modulates heat shock-induced programmed cell death in Arabidopsis. New Phytol 195:85–96
Li Y, Chen L, Mu J, Zuo J (2013) LESION SIMULATING DISEASE1 interacts with catalases to regulate hypersensitive cell death in Arabidopsis. Plant Physiol 163:1059–1070
Lin J, Wang Y, Wang G (2005) Salt stress-induced programmed cell death via Ca2+ -mediated mitochondrial permeability transition in tobacco protoplasts. Plant Growth Reg 45:243–250
Lin J, Wang Y, Wang G (2006) Salt stress-induced programmed cell death in tobacco protoplasts is mediated by reactive oxygen species and mitochondrial permeability transition pore status. J Plant Physiol 163:731–739
Liu K, Shen L, Wang J, Sheng J (2008) Rapid inactivation of chloroplastic ascorbate peroxidase is responsible for oxidative modification to rubisco in Tomato (Lycopersicon esculentum) under cadmium stress. J Integr Plant Biol 50:415–426
Liu J, Li Z, Wang Y, Xing D (2014) Overexpression of ALTERNATIVE OXIDASE1a alleviates mitochondria-dependent programmed cell death induced by aluminium phytotoxicity in Arabidopsis. J Exp Bot 65:4465–4478
Lyubushkina IV, Grabelnych OI, Pobezhimova TP, Stepanov AV, Fedyaeva AV, Fedoseeva IV, Voinikov VK (2014) Winter wheat cells subjected to freezing temperature undergo death process with features of programmed cell death. Protoplasma 251:615–623
Ma W, Xu W, Xu H, Chen Y, He Z, Ma M (2010) Nitric oxide modulates cadmium in influx during cadmium-induced programmed cell death in tobacco BY-2 cells. Planta 232:325–335
Mateo A, Muhlenbock P, Rusterucci C, Chang C, Miszalski Z, Karpinska B, Parker J, Mullineaux PM, Karpinski S (2004) LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136:2818–2830
Mazel A, Levine A (2001) Induction of cell death in Arabidopsis by superoxide in combination with salicylic acid or with protein synthesis inhibitors. Free Rad Biol Med 30:98–106
Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annl Rev Plant Biol 61:443–462
Mizuno M, Tada Y, Uchii K, Kawakami S, Mayama S (2005) Catalase and alternative oxidase cooperatively regulate programmed cell death induced by beta-glucan elicitor in potato suspension cultures. Planta 220:849–853
Monetti E, Kadono T, Tran D, Azzarello E, Arbelet-bonnin D, Biligui B, Briand J, Kawano T, Mancuso S, Bouteau F (2014) Deciphering early events involved in hyperosmotic stress-induced programmed cell death in tobacco BY-2 cells. J Exp Bot 65:1361–1375
Mühlenbock P, Szechynska-Hebda M, Plaszczyca M, Baudo M, Mateo A, Mullineaux PM, Parker JE, Karpinska B, Karpinski S (2008) Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell 20:2339–2356
Overmyer K, Brosche M, Pellinen R, Kuittinen T, Tuominen H, Ahlfors R, Keinanen M, Saarma M, Scheel D, Kangasjarvi J (2005) Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1 mutant. Plant Physiol 137:1092–1104
Peters JS, Chin C (2005) Evidence for cytochrome f involvement in eggplant cell death induced by palmitoleic acid. Cell Death Different 12:405–407
Petrov V, Hille J, Mueller-roeber B, Gechev TS (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Front Plant Sci 6:69
Polle A (2001) Dissecting the superoxide dismutase-ascorbate-glutathione pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiol 126:445–462
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
Rezaei A, Amirjani M, Mahdiyeh M (2013) Programmed cell death induced by salt stress in wheat cell suspension. Int J Forest Soil Eros 3:35–39
Robinson JM, Bunce JA (2000) Influence of drought-induced water stress on soybean and spinach leaf ascorbate-dehydroascorbate level and redox Status. Int J Plant Sci 161:271–279
Robson CA, Vanlerberghe GC (2002) Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and-independent pathways of programmed cell death. Plant Physiol 129:1908–1920
Samuilov VD, Lagunova EM, Gostimsky SA, Timofeev KN, Gusev MV (2003) Role of chloroplast photosystems II and I in apoptosis of pea guard cells. Biochemistry (Mosc) 68:912–917
Sewelam N, Kazan K, Schenk PM (2016) Global plant stress signaling: reactive oxygen species at the cross-road. Front Plant Sci 7:187
Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–1665
Shabala S, Cuin TA, Prismall L, Nemchinov LG (2007) Expression of animal CED-9 anti-apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress. Planta 227:189–197
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
Tamaoki M (2008) The role of phytohormone signaling in ozone—induced cell death in plants. Plant Signal Behav 3:166–174
Tamaoki M, Nakajima N, Kubo A, Aono M, Matsuyama T, Saji H (2003) Transcriptome analysis of O3-exposed Arabidopsis reveals that multiple signal pathways act mutually antagonistically to induce gene expression. Plant Mol Biol 53:443–456
Tata JR (1966) Requirment for RNA and protein synthesis for induction regression of the tadpole tail in organ culture. Dev Biol 13:77–94
Thomas SG, Franklin-Tong VE (2004) Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429:305–309
Torres MA, Jones JD, Dangl JL (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 37:1130–1134
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
Van Aken O, Van Breusegem F (2015) Licensed to kill: mitochondria, chloroplasts, and cell death. Trend Plant Sci 20:754–766
Van Aken O, Giraud E, Clifton R, Whelan J (2009) Alternative oxidase: a target and regulator of stress responses. Physiol Planta 137:354–361
Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390
Vandenabeele S, Van Der Kelen K, Dat J, Gadjev I, Boonefaes T, Morsa S, Rottiers P, Slooten L, Van Montagu M, Zabeau M, Inze D, Van Breusegem F (2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc Nat Acad Sci U S A 100:16113–16118
Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci 14:6805–6847
Vavilala SL, Gawde KK, Sinha M, Souza JS (2015) Programmed cell death is induced by hydrogen peroxide but not by excessive ionic stress of sodium chloride in the unicellular green alga Chlamydomonas reinhardtii. Eur J Phycol 50:422–438
Wang W, Pan J, Zheng K, Chen H, Shao H, Guo Y, Bian H, Han N, Wang J, Zhu M (2009) Ced-9 inhibits Al-induced programmed cell death and promotes Al tolerance in tobacco. Biochem Biophys Res Commun 383:141–145
Wang J, Li X, Liu Y, Zhao X (2010) Salt stress induces programmed cell death in Thellungiella halophila suspension-cultured cells. J Plant Physiol 167:1145–1151
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. Nat Sci Rep 4:5989
Watanabe N, Lam E (2006) Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death. Plant J 45:884–894
Wituszynska W, Karpinski S (2013) Programmed cell death as a response to high light, UV and drought stress in plants. In: Abiotic stress-plant response and application in agriculture. InTech Publisher, pp 207–246
Xu P, Rogers SJ, Roossinck MJ (2004) Expression of antiapoptotic genes bcl-xL and ced-9 in tomato enhances tolerance to viral-induced necrosis and abiotic stress. Proc Nat Acad Sci U S A 101:15805–15810
Xu H, Xu W, Xi H, Ma W, He Z, Ma M (2013) The ER luminal binding protein (BiP) alleviates Cd2+—induced programmed cell death through endoplasmic reticulum stress—cell death signaling pathway in tobacco cells. Plant Physiol 170:1434–1441
Yao N, Greenberg JT (2006) Arabidopsis ACCELERATED CELL DEATH2 modulates programmed cell death. Plant Cell 18:397–411
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
Zhang X, Liu S, Takano T (2008) Two cysteine proteinase inhibitors from Arabidopsis thaliana, AtCYSa and AtCYSb, increasing the salt, drought, oxidation and cold tolerance. Plant Mol Biol 68:131–143
Zhang L, Li Y, Xing D, Gao C (2009) Characterization of mitochondrial dynamics and subcellular localization of ROS reveal that HsfA2 alleviates oxidative damage caused by heat stress in Arabidopsis. J Exp Bot 60:2073–2091
Zhang D, Liu D, Lv X, Wang Y, Xun Z, Liu Z, Li F, Lu H (2014) The cysteine protease CEP1, a key executor involved in tapetal programmed cell death, regulates pollen development in Arabidopsis. Plant Cell 26:2939–2961
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
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Kumar, S.R., Mohanapriya, G., Sathishkumar, R. (2016). Abiotic Stress-Induced Redox Changes and Programmed Cell Death in Plants—A Path to Survival or Death?. In: Gupta, D., Palma, J., Corpas, F. (eds) Redox State as a Central Regulator of Plant-Cell Stress Responses. Springer, Cham. https://doi.org/10.1007/978-3-319-44081-1_11
Download citation
DOI: https://doi.org/10.1007/978-3-319-44081-1_11
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-44080-4
Online ISBN: 978-3-319-44081-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)