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Nitric Oxide in Plants: Metabolism and Role in Stress Physiology pp 281–296Cite as

The Role of Nitric Oxide in Programmed Cell Death in Higher Plants

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Abstract

Programmed cell death (PCD) is a genetically controlled biological process involved in defense, development, and stress response. Generally, the characters of plant PCD are similar to animal apoptosis, for instance cytoplasm shrinkage, chromatin condensation, and DNA fragmentation. An important signaling molecule, nitric oxide (NO) has been implicated in environmental-induced plant PCD, but its signaling and controlling network is still unknown. Whether NO promotes or suppresses PCD depends on NO sources and concentration in different plant species and environmental conditions. The effects of NO on developmental PCD were extensively studied. NO not only plays a crucial role in hypersensitive response (HR) during plant-pathogen interactions, but is also involved in abiotic stress-induced PCD including heat shock, salt, drought, cold, UV radiation, ozone, and heavy metals (mainly cadmium, aluminum). Previous studies showed the mitochondrion as a modulating center of PCD and also control NO level in planta. Vacuole processing enzyme (VPE) and caspase-like protein are involved in PCD. NO regulates the expression of PCD-associated genes via mitogen-activated protein kinase (MAPK) cascade, S-nitrosylation, and cGMP-dependent pathway. In addition, there are diverse interactions between NO and other signals such as hydrogen peroxide, calcium, ethylene, and salicylic acid (SA) during PCD. Based on understanding of related knowledge, NO signaling network in response to PCD in higher plants is presented in this chapter.

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References

  • Ahlfors R, Brosche M, Kollist1 H et al (2009a) Nitric oxide modulates ozone-induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana. Plant J 58: 1–12

    Google Scholar 

  • Ahlfors R, Brosche M, Kangasjarvi J (2009b) Ozone and nitric oxide interaction in Arabidopsis thaliana. Plant Signaling & Behavior 4:878–879

    Article  CAS  Google Scholar 

  • Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Deckert J et al (2012) Nitric oxide implication in cadmium-induced programmed cell death in roots and signaling response of yellow lupine plants. Plant Physiol Biochem 58:124–134

    Article  CAS  PubMed  Google Scholar 

  • Asai T, Tena G, Plotnikova J et al (2002) MAP kinase signaling cascade in Arabidopsis innate immunity. Nature 415:977–983

    Article  CAS  PubMed  Google Scholar 

  • Attia K, Li KG, Wei C et al (2005) Overexpression of OsPDCD5 gene induces programmed cell death in rice. J Integr Plant Biol 47:1115–1122

    Article  CAS  Google Scholar 

  • Beligni MV, Fath A, Bethke PC et al (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol 129:1642–1650

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brotner CD, Oldenburg NBE, Cidlowski JA (1995) The role of DNA fragmentation in apoptosis. Clinical Cancer Res 11:21–26

    Google Scholar 

  • Chen X, Wang Y, Li JY et al (2009) Mitochondrial proteome during salt stress-induced programmed cell death in rice. Plant Physiol Biochem 47:407–415

    Article  CAS  PubMed  Google Scholar 

  • Clarke A, Desikan R, Hurst RD et al (2000) NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant J 24:667–677

    Article  CAS  PubMed  Google Scholar 

  • Crawford NM (2006) Mechanisms for nitric oxide synthesis in plants. J Exp Bot 57:471–478

    Article  CAS  PubMed  Google Scholar 

  • Cverkovska M, Vanlerberghe GC (2012) Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytol 195:32–39

    Article  Google Scholar 

  • Delledonne M, Zeier J, Marocco A et al (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98:13454–13459

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • De Michele R, Vurro E, Rigo C et al (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217–228

    Article  PubMed Central  PubMed  Google Scholar 

  • De Pinto MC, Tommasi F, Gara LD (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco Bright-Yellow 2 cells. Plant Physiol 130:698–708

    Article  PubMed Central  PubMed  Google Scholar 

  • Desikan R, Griffiths R, Hancock J et al (2002) A new role for an old enzyme: Nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci USA 99:16314–16318

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95:10328–10333

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ederli L, Morettini R, Borgogni A et al (2006) Interaction between nitric oxide and ethylene in the induction of alternative oxidase in ozone-treated tobacco plants. Plant Physiol 142:595–608

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ederli L, Reale L, Madeo L et al (2009) NO release by nitric oxide donors in vitro and in planta. Plant Physiol Biochem 47:42–48

    Article  CAS  PubMed  Google Scholar 

  • Gabaldon C, Ros Gomez LV, Pedrefio MA et al (2005) Nitric oxide production by the differentiating xylem of Zinnia elegant. New Phytol 165:121–130

    Article  CAS  PubMed  Google Scholar 

  • Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:450–493

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ 27:521–549

    Article  CAS  Google Scholar 

  • Gupta KJ, Shah JK, Brotman Y et al (2012) Inhibition of aconitase by nitric oxide leads to induction of alternative oxidase and to a shift of metabolism towards biosynthesis of amino acids. J Exp Bot 63:1773–1784

    Article  CAS  PubMed  Google Scholar 

  • Hatsugai N, Kuroyanagi M, Yamada K et al (2004) A plant vacuole protease, VPE, mediates virus-induced hypersensitive cell death. Science 305:855–858

    Article  CAS  PubMed  Google Scholar 

  • Huckelhoven R (2004) BAX Inhibitor-1, an ancient cell death suppressor in animals and plants with prokaryotic relatives. Apoptosis 9:299–307

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Kolodziejek I, Koziol-Lipinska J, Waleza M et al (2007) Aspects of programmed cell death during early senescence of barley leaves: possible role of nitric oxide. Protoplasma 232:97–108

    Article  CAS  PubMed  Google Scholar 

  • Kumar KRR, Kirti PB (2010) A mitogen-activated protein kinase genes, AhMPK6 from peanut localizes to the nucleus and also induces defense responses upon transient expression in tobacco. Plant Physiol Biochem 48:481–486

    Article  CAS  PubMed  Google Scholar 

  • Kumar KRR, Srinivasan T, Kirti PB (2009) A mitogen-activated protein kinase genes, AhMPK3 of peanut: molecular cloning, genomic organization, and heterologous expression conferring resistance against Spodoptera litura in tobacco. Mol Genet Genomics 282:65–81

    Article  CAS  PubMed  Google Scholar 

  • Kuthanova A, Opatrny Z, Fischer L (2008) Is internucleosomal DNA fragmentation an indicator of programmed death in plant cells? J Exp Bot 59:2233–2240

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lamattina L, Garcia-Mata C, Graziano M et al (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–139

    Article  CAS  PubMed  Google Scholar 

  • Lanteri M, Pagnussat GC, Lamattina L (2006) Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. J Exp Bot 57:1341–1351

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Xing D (2011) Mechanistic study of mitochondria-dependent programmed cell death induced by aluminum phytotoxicity using fluorescence techniques. J Exp Bot 62:331–343

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Yue HY, 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

    Article  CAS  PubMed  Google Scholar 

  • Lin AH, Wang YQ, Tang JY (2011) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide induced leaf cell death in rice. Plant Physiol 158:451–464

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu HT, Wang YG, Zhang YM (1999) TFAR19, a novel apoptosis-related gene cloned from human leukemia cell line TF-1 could enhance apoptosis of some tumor cells induced by growth factor withdraw. Biochem Biophys Res Commun 245:203–210

    Article  Google Scholar 

  • Lombardi L, Ceccarelli N, Picciarelli P et al (2010) Nitric oxide and hydrogen peroxide involvement during programmed cell death of Sechium edule nucellus. Physiol Plant 140:89–102

    Article  CAS  PubMed  Google Scholar 

  • Malerba M, Contran N, Tonelli M et al (2008) Role of nitric oxide in actin depolymerization and programmed cell death induced by fusicoccin in sycamore (Acer pseudoplatanus) cultured cells. Physiol Plant 133:449–457

    Article  CAS  PubMed  Google Scholar 

  • Ma WW, Xu WZ, Xu H et al (2010) Nitric oxide modulates cadmium influx during cadmium-induced programmed cell death in tobacco BY-2 cells. Planta 232:325–335

    Article  CAS  PubMed  Google Scholar 

  • Murgia I, de Pinto MC, Delledonne M et al (2004) Comparative effects of various nitric oxide donors on ferritin regulation, programmed cell death, and cell redox state in plant cells. J Plant Physiol 161:777–783

    Article  CAS  PubMed  Google Scholar 

  • Neill S (2005) NO way to die – nitric oxide, programmed cell death and xylogenesis. New Phytol 165:1–2

    Google Scholar 

  • Overmyer K, Brosche M, Kangasjarvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342

    Article  CAS  PubMed  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the IAA-induced adventitious rooting process. Plant Physiol 132:1241–1248

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lombardo MC et al (2004) Nitric oxide mediats the indole acetic acid induction of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135:279–286

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ren DT, Yang HP, Zhang SQ (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem 277:559–565

    Article  CAS  PubMed  Google Scholar 

  • Robson C, Vanlerberghe G (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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Seo S, Okamoto M, Seto H et al (1995) Tobacco MAP kinase: a possible mediator in wound signal transduction pathway. Science 270:1988–1992

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Van Aken O, Giraud E, Clifton R et al (2009) Alternative oxidase: a target and regulator of stress responses. Physiol Plant 137:354–361

    Article  PubMed  Google Scholar 

  • Vlot AC, Klessig DF, Park SW (2008) Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol 11:436–442

    Article  CAS  PubMed  Google Scholar 

  • Wang PC, Du YY, Li Y (2010a) Hydrogen peroxide-mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell 22:2981–2998

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang WZ, Pan JW, Zheng K et al (2009) Ced-9 inhibits Al-induced programmed cell death and promotes Al tolerance in tobacco. Biochem Biophys Res Commun 383:141–145

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Lin JS, Wang GX (2010b) Role of calcium in nitric oxide-induced programmed cell death in tobacco protoplasts. Biol Plant 54:471–476

    Article  CAS  Google Scholar 

  • Wang YQ, Chen C, Loake GL et al (2010c) Nitric oxide: promoter or suppressor of programmed cell death? Protein Cell 1:133–142

    Article  CAS  PubMed  Google Scholar 

  • Wilkins KA, Bancroff J, Bosch M et al (2011) Reactive oxygen species and nitric oxide mediate actin reorganization and programmed cell death in the self-incompatibility response of papaver. Plant Physiol 156:404–416

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wulff A, Oliveira HC, Saviani EE et al (2009) Nitrite reduction and superoxide-dependent nitric oxide degradation by Arabidopsis mitochondria: Influence of external NAD(P)H dehydrogenases and alternative oxidase in the control of nitric oxide levels. Nitric Oxide 21:132–139

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, Fu G, Yang YJ et al (2011) Tungstate: is it really a specific nitrate reductase inhibitor in plant nitric oxide research? J Exp Bot 63:33–41

    Article  PubMed  Google Scholar 

  • Ye Y, Li Z, Xing D et al (2012) Sorting out the role of nitric oxide in cadmium-induced Arabidopsis thaliana programmed cell death. Plant Signaling & Behavior 7:1493–1494

    Article  Google Scholar 

  • Ye Y, Li Z, Xing D (2013) Nitric oxide promotes MPK6-mediated caspase-3-like activation in cadmium-induced Arabidopsis thaliana programmed cell death. Plant, Cell Environ 36:1–15

    Article  CAS  Google Scholar 

  • Zago E, Morsa S, Dat JF (2006) Nitric oxide- and hydrogen peroxide- responsive gene regulation during cell death induction in tobacco. Plant Physiol 141:404–411

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhan J, He HY, Wang TJ et al (2013) Aluminum-induced programmed cell death promoted by AhSAG, a senescence-associated gene in Arachis hypoganea L. Plant Sci 210:108–117

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Czymmek KJ, Shapiro AD (2003) Nitric oxide does not trigger early programmed cell death events but may contribute to cell-to-cell signaling governing progression of the Arabidopsis hypersensitive response. MPMI 16:962–972

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Fujita K, Sakai K (2007) Reactive oxygen species, nitric oxide, and their interactions play different roles in Cupressus lusitanica Cell death and phytoalexin biosynthesis. New Phytol 175:215–229

    Article  CAS  PubMed  Google Scholar 

  • Zheng K, Pan JW, Ye L et al (2007) Programmed cell death-involved aluminum toxicity in yeast alleviated by antiapoptotic members with decreased calcium signals. Plant Physiol 143:38–49

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Foundation of China (31260296, 30960181, 30560070).

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Authors and Affiliations

  1. College of Agronomy, Guangxi University, Nanning, 530004, People’s Republic of China

    Hu-Yi He, Ming-Hua Gu & Long-Fei He

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  1. Hu-Yi He
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  2. Ming-Hua Gu
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  3. Long-Fei He
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Correspondence to Long-Fei He .

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Editors and Affiliations

  1. Faculty of Science, Department of Biology, University of Tabuk, Tabuk, Saudi Arabia

    M. Nasir Khan

  2. Faculty of Science, Department of Biology, University of Tabuk, Tabuk, Saudi Arabia

    Mohammad Mobin

  3. Plant Physiology Section,Department of Botany, Aligarh Muslim University, Aligarh, India

    Firoz Mohammad

  4. Departamento de Bioquímica Biol. Cellular y Molecular de Plantas, Estación Experimental del Zaidín Consejo Superior de Investigaciones Científicas, Granada, Spain

    Francisco J. Corpas

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He, HY., Gu, MH., He, LF. (2014). The Role of Nitric Oxide in Programmed Cell Death in Higher Plants. In: Khan, M., Mobin, M., Mohammad, F., Corpas, F. (eds) Nitric Oxide in Plants: Metabolism and Role in Stress Physiology. Springer, Cham. https://doi.org/10.1007/978-3-319-06710-0_17

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