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Plastid Development in Leaves during Growth and Senescence pp 529–550Cite as

Chloroplast Control of Leaf Senescence

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Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 36))

Summary

Chloroplasts have an active role in the induction and course of senescence through signals, derived from reactive oxygen species (ROS), exiting to the cytosol. In this way, leaf chloroplasts mimic the role of mitochondria in the apoptosis of non-photosynthetic organs. Oxylipins, magnesium-protoporphyrin IX (Mg-ProtoIX) and proteins are the best studied signal candidates that exit from chloroplasts that, through a poorly-understood network of transduction intermediates, inhibit the expression of genes encoding components of the photosynthetic machinery and activate the expression of senescence-associated genes (SAG) in the nucleus, ultimately resulting in activation of programmed cell death (PCD). There are many similarities in the mechanisms of production and scavenging of ROS in chloroplasts during stress defense and in senescence. However, there are also differences and one significant difference is that the feed-back effect of chloroplast signals on the ROS level in defense responses changes to a feed-forward effect that favors further increases of ROS in the PCD associated with leaf senescence or the hypersensitive response (HR). Therefore, a key question related to the induction of leaf senescence resides in the molecular basis of the shift from a feed-back to a feed-forward suicide response of the network that regulates the chloroplast ROS level. Up-regulation of nuclear genes encoding components of the thylakoid Ndh complex and of lipoxygenase (LX) and down-regulation of the nuclear genes for chloroplastic superoxide dismutase (SOD) seem to be among the changes responsible for the feed-forward increase of ROS associated with (and probably determining) PCD, but further investigations are needed to identify the intermediates and their cause-effect relations in the signal transduction network. These investigations must include hormones, H2O2, proteins and microRNAs, whose levels and interactions are also affected by environmental factors acting inside and outside the chloroplast.

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Abbreviations

ABA:

Abscisic acid;

3Chl*:

Triplet excited chlorophyll;

Csd2 :

Gene encoding the chloroplastic Cu/ZnSOD;

HR:

Hypersensible response;

JA:

Jasmonic acid and derivatives;

LX:

Lipoxygenase;

Mg-ProtoIX:

Magnesium-protoporphyrin IX;

Ndh:

Thylakoid NADH dehydrogenase complex;

ndh – :

Genes for components of the thylakoid Ndh complex;

NPQ:

Non-photochemical quenching;

1O2 :

Singlet oxygen;

O2•− :

Superoxide anion radical;

PCD:

Programmed cell death;

PET:

Photosynthetic electron transport;

POS:

Photooxidative stress;

PPR:

Pentatricopeptide-repeat;

PRDX:

Peroxiredoxin;

PSI (II):

Photosystem I (II);

PX:

Peroxidase;

ROS:

Reactive oxygen species;

SAG:

Senescence-associated genes;

SAR:

Systemic acquired resistance;

SOD:

Superoxide dismutase;

TO:

Terminal oxidase

References

  • Abarca D, Martín M, Sabater B (2001a) Differential leaf stress responses in young and senescent plants. Physiol Plant 113:409–415

    Article  PubMed  CAS  Google Scholar 

  • Abarca D, Roldán M, Martín M, Sabater B (2001b) Arabidopsis thaliana ecotype Cvi shows an increased tolerance to photo-oxidative stress and contains a new chloroplastic copper/zinc superoxide dismutase isoenzyme. J Exp Bot 52:1417–1425

    Article  PubMed  CAS  Google Scholar 

  • Ankele E, Kindgren P, Pesquet E, Strand A (2007) In vivo visualization of Mg-protoporphyrin IX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast. Plant Cell 19:1964–1979

    Article  PubMed  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–379

    Article  PubMed  CAS  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  PubMed  CAS  Google Scholar 

  • Bachmann A, Hause B, Maucher H, Garbe E, VörÖs K, Weicher H, Wasternack C, Feussner I (2002) Jasmonate-induced lipid peroxidation in barley leaves initiated by distinct 13-LOX forms of chloroplasts. Biol Chem 383:1645–1657

    Article  PubMed  CAS  Google Scholar 

  • Bailey-Serres J, Rochaix JD, Wassenegger M, Filipowicz W (1999) Plants, their organelles, viruses and transgenes reveal the mechanisms and relevance of post-transcriptional processes. EMBO J 18:5153–5158

    Article  PubMed  CAS  Google Scholar 

  • Barkan A, Goldschmidt-Clermont M (2000) Partici­pation of nuclear genes in chloroplast gene expression. Biochimie 82:559–572

    Article  PubMed  CAS  Google Scholar 

  • Bate NJ, Rothstein EJ, Thompson JE (1991) Expression of nuclear and chloroplast photosynthesis-specific genes during leaf senescence. J Exp Bot 42:801–811

    Article  CAS  Google Scholar 

  • Becker W, Apel K (1993) Differences in gene expression between natural and artificially induced leaf senescence. Planta 189:74–79

    Article  CAS  Google Scholar 

  • Beevers L (1976) Senescence. In: Bonner J, Varner JE (eds) Plant biochemistry. Academic, New York, pp 771–794

    Google Scholar 

  • Behera SK, Nayak L, Biswal B (2003) Senescing leaves possess potential for stress adaptation: developing leaves acclimated to high light resist osmotic stress during senescence. J Plant Physiol 160:125–131

    Article  PubMed  CAS  Google Scholar 

  • Beick S, Schmitz-Linneweber C, Williams-Carrier R, Jensen B, Barkan A (2008) The pentatricopeptide repeat protein PPR5 stabilizes a specific tRNA precursor in maize chloroplasts. Mol Cell Biol 28:5337–5347

    Article  PubMed  CAS  Google Scholar 

  • Biehler K, Fock H (1996) Evidence for the contribution of the Mehler-peroxidase reaction in dissipating excess electrons in drought-stressed wheat. Plant Physiol 112:265–272

    PubMed  CAS  Google Scholar 

  • Biswal B, Biswal UC (1999) Leaf senescence, its physiology and molecular biology. Curr Sci 77:775–782

    CAS  Google Scholar 

  • Bowler C, Van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    Article  CAS  Google Scholar 

  • Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48:181–199

    Article  Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Pyung OL, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver C (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585

    Article  PubMed  CAS  Google Scholar 

  • Burgess DG, Taylor WC (1987) Chloroplast photooxidation affects the accumulation of cytosolic mRNAs encoding chloroplast proteins in maize. Planta 170:520–527

    Article  CAS  Google Scholar 

  • Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17:868–876

    Article  PubMed  CAS  Google Scholar 

  • Casano LM, Martín M, Sabater B (1994) Sensitivity of superoxide dismutase transcript levels and activities to oxidative stress is lower in mature-senescent than in young barley leaves. Plant Physiol 106:1033–1039

    PubMed  CAS  Google Scholar 

  • Casano LM, Martín M, Zapata JM, Sabater B (1999) Leaf age- and paraquat-dependent effects on the levels of enzymes protecting against photooxidative stress. Plant Sci 149:13–22

    Article  CAS  Google Scholar 

  • Casano LM, Zapata JM, Martín M, Sabater B (2000) Chlororespiration and poising of cyclic electron transport: plastoquinone as electron transporter between thylakoid NADH dehydrogenase and peroxidase. J Biol Chem 275:942–948

    Article  PubMed  CAS  Google Scholar 

  • Casano LM, Martín M, Sabater B (2001) Hydrogen peroxide mediates the induction of chloroplastic Ndh complex under photooxidative stress in barley. Plant Physiol 125:1450–1458

    Article  PubMed  CAS  Google Scholar 

  • Catalá R, Sabater B, Guéra A (1997) Expression of the plastid ndhF gene product in photosynthetic and non-photosynthetic tissues of developing barley seedlings. Plant Cell Physiol 38:1382–1388

    Article  PubMed  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Chen GH, Huang LT, Yap MN, Lee RH, Huang YJ, Cheng MC, Chen SCG (2002a) Molecular characterization of a senescence-associated gene encoding cysteine proteinase and its gene expression during leaf senescence in sweet potato. Plant Cell Physiol 43:984–991

    Article  PubMed  CAS  Google Scholar 

  • Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA, Budworth PR, Tao Y, Xie Z, Chen X, Lam S, Kreps JA, Harper JF, Si-Ammour A, Mauch-Mani B, Heinlein M, Kobayashi K, Hohn T, Dangl JL, Wang X, Zhu T (2002b) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574

    Article  PubMed  CAS  Google Scholar 

  • Chen S, Yin C, Qiang S, Zhou F, Dai X (2010) Chloroplastic oxidative burst induced by tenuazonic acid, a natural photosynthesis inhibitor, trigger cell necrosis in Eupatorium adenophorum Spreng. Biochim Biophys Acta 1797:391–405

    Article  PubMed  CAS  Google Scholar 

  • Creelman RA, Mulpuri R (2002) The oxylipin pathway in Arabidopsis. The Arabidopsis Book. http://www.aspb.org/publications/arabidopsis/. American Society of Plant Physiologists, Rockville, pp 1–24

  • Cuello J, Quiles MJ, Rosauro J, Sabater B (1995) Effects of growth regulators and light on chloroplast NAD(P)H dehydrogenase activities of senescent barley leaves. Plant Growth Regul 17:225–232

    Article  CAS  Google Scholar 

  • Dalling MJ (1985) The physiological basis of nitrogen redistribution during grain filling in cereals. In: Harper JE, Schrader LE, Howell RW (eds) Exploitation of physiological and genetic variability to enhance crop productivity. American Society of Plant Physiologists, Rockville, pp 55–71

    Google Scholar 

  • Daniel X, Lacomme C, Morel JB, Roby D (1999) A novel myb oncogene homologue in Arabidopsis thaliana related to hypersensitive cell death. Plant J 20:57–66

    Article  PubMed  CAS  Google Scholar 

  • Darehshouri A, Lutz-Meindl U (2010) H2O2 localization in the green alga Micrasterias after salt and osmotic stress by TEM-coupled electron energy loss spectroscopy. Protoplasma 239:49–56

    Article  PubMed  CAS  Google Scholar 

  • Del Campo EM, Sabater B, Martín M (2000) Transcripts of the ndhH-D operon of barley plastids: possible role of unedited site III in splicing of the ndhA intron. Nucleic Acids Res 28:1092–1098

    Article  PubMed  Google Scholar 

  • Del Campo EM, Sabater B, Martín M (2002) Post-transcriptional control of chloroplast gene expression: accumulation of stable psaC mRNA is due to downstream RNA cleavages in the ndhD gene. J Biol Chem 277:36457–36464

    Article  PubMed  CAS  Google Scholar 

  • Del Campo EM, Sabater B, Martín M (2006) Characterization of the 5′- and 3′-ends of mRNAs of ndhH, ndhA and ndhI genes of the plastid ndhH-D operon. Biochimie 88:347–357

    Article  CAS  Google Scholar 

  • Del Río LA, Pastori GM, Palma JM, Sandalio LM, Sevilla F, Corpas FJ, Jiménez A, López-Huertas E, Hernández JA (1998) The activated oxygen role of peroxisomes in senescence. Plant Physiol 116:1195–1200

    Article  PubMed  Google Scholar 

  • Demetrius L, Manke T (2005) Robustness and network evolution – and entropy principle. Physica A 346:682–696

    Article  Google Scholar 

  • Deo PM, Biswal UC, Biswal B (2006) Water stress sensitized photoinhibition in senescing cotyledons of clusterbean: changes in thylakoid structure and inactivation of photosystem II. Photosynthetica 44:187–192

    Article  CAS  Google Scholar 

  • Desveaux D, Maréchal A, Brisson N (2005) Whirly transcription factors: defense gene regulation and beyond. Trends Plant Sci 10:95–102

    Article  PubMed  CAS  Google Scholar 

  • Dhinsa RS, Plumb-Dhinsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    Article  Google Scholar 

  • Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107

    Article  PubMed  CAS  Google Scholar 

  • Ding YH, Liu NY, Tang ZS, Liu J, Yang WC (2006) Arabidopsis glutamine-rich protein22 is essential for early embryogenesis and encodes a novel nuclear PPR motif protein that interacts with RNA polymerase II subunit III. Plant Cell 18:815–830

    Article  PubMed  CAS  Google Scholar 

  • Douce R, Heldt HW (2000) Photorespiration. In: Leegood RC, Sharkey TD, Von Caemmerer S (eds) Photosynthesis: physiology and metabolism. Kluwer, Dordrecht, pp 115–136

    Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Endo T, Shikanai T, Takabayashi A, Asada K, Sato F (1999) The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett 457:5–8

    Article  PubMed  CAS  Google Scholar 

  • Epple P, Mack AA, Morris VRF, Dangl JL (2003) Antagonistic control of oxidative stress-induced cell death in Arabidopsis by two related, plant-specific zinc finger proteins. Proc Natl Acad Sci USA 100:6831–6836

    Article  PubMed  CAS  Google Scholar 

  • Eskling M, Emanuelsson A, Akerlund HE (2001) Enzyme and mechanisms for violaxanthin-zeaxanthin conversions. In: Aro EM, Andersson B (eds) Regulation of photosynthesis. Kluwer, Dordrecht, pp 433–452

    Google Scholar 

  • Eulgem T (2005) Regulation of Arabidopsis defense transcriptome. Trends Plant Sci 10:71–78

    Article  CAS  PubMed  Google Scholar 

  • Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206

    Article  PubMed  CAS  Google Scholar 

  • Eze JMO, Dumbroff EB, Thompson JE (1981) Effects of moisture stress and senescence on the synthesis of abscisic acid in the primary leaves of bean. Physiol Plant 51:418–422

    Article  CAS  Google Scholar 

  • Favory JJ, Kobayshi M, Tanaka K, Peltier G, Kreis M, Valay JG, Lerbs-Mache S (2005) Specific function of a plastid sigma factor for ndhF gene transcription. Nucleic Acids Res 33:5991–5999

    Article  PubMed  CAS  Google Scholar 

  • Felder S, Meierhoff K, Sane AP, Meurer J, Driemel C, Plücken H, Klaff P, Stein B, Bechtold N, Westhoff P (2001) The nucleus-encoded HCF107 gene of Arabidopsis provides a link between intercistronic RNA processing and the accumulation of translation-competent psbH transcripts in chloroplasts. Plant Cell 13:2127–2141

    PubMed  CAS  Google Scholar 

  • Feller U, Fischer A (1994) Nitrogen metabolism in senescing leaves. Cr Rev Plant Sci 13:241–273

    CAS  Google Scholar 

  • Fernández AP, Strand Å (2008) Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Curr Opin Plant Biol 11:509–513

    Article  PubMed  CAS  Google Scholar 

  • Fischer-Kilbienski I, Miao Y, Roitsch T, Zschiesche W, Humbeck K, Krupinska K (2010) Nuclear targeted AtS40 modulates senescence associated gene expression in Arabidopsis thaliana during natural development and in darkness. Plant Mol Biol 73:379–390

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • García S, Martín M, Sabater B (1983) Protein synthesis by chloroplasts during the senescence of leaves. Physiol Plant 57:260–266

    Article  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Guéra A, Martín M, Sabater B (1989) Subchloroplast localization of polypeptides synthesized by chloroplasts during senescence. Physiol Plant 75:382–388

    Article  Google Scholar 

  • Guo Y, Gan S (2006) AtNAP, a NAC family transcription factors, has an important role in leaf senescence. Plant J 46:601–612

    Article  PubMed  CAS  Google Scholar 

  • Guo XX, Yan XQ, Yang RY, Zeng QP (2010) Salicylic acid and methyl jasmonate but not Rose Bengal enhance artemisinin production through invoking burst of endogen singlet oxygen. Plant Sci 178:390–397

    Article  CAS  Google Scholar 

  • Hayden DM, Christopher DA (2004) Characterization of senescence-associated gene expression and senescence-dependent and -independent cysteine proteases differing in microsomal processing in Anthurium. Plant Sci 166:779–790

    Article  CAS  Google Scholar 

  • He Y, Gan S (2002) A gene encoding an acyl hydrolase is involved in leaf senescence in Arabidopsis. Plant Cell 14:805–815

    Article  PubMed  CAS  Google Scholar 

  • He CJ, Morgan PW, Drew MC (1996) Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiol 112:463–472

    PubMed  CAS  Google Scholar 

  • Heber U, Walker D (1992) Concerning a dual function of coupled cyclic electron transport in leaves. Plant Physiol 100:1621–1626

    Article  PubMed  CAS  Google Scholar 

  • Hu XJ, Zhang ZB, Xu P, Fu ZY, Hu SB, Song WY (2010) Multifunctional genes: the cross-talk among the regulation networks of abiotic stress responses. Biol Plant 54:213–223

    Article  CAS  Google Scholar 

  • Huang M, Braun DM (2010) Genetic analyses of cell death in maize (Zea mays, Poaceae) leaves reveal a distinct pathway operating in the camouflage1 mutant. Am J Bot 97:357–364

    Article  PubMed  CAS  Google Scholar 

  • Hung KT, Hsu YT, Kao CH (2006) Hydrogen peroxide is involved in methyl jasmonate-induced senescence of rice leaves. Physiol Plant 127:293–303

    Article  CAS  Google Scholar 

  • Jayabaskaran C, Kuntz M, Guillemaut P, Weil JH (1990) Variations in the levels of chloroplast tRNAs and aminoacyl-tRNA synthetases in senescing leaves of Phaseolus vulgaris. Plant Physiol 92:136–140

    Article  PubMed  CAS  Google Scholar 

  • Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J 22:6150–6161

    Article  Google Scholar 

  • Joët T, Cournac L, Peltier G, Havaux M (2002) Cyclic electron flow around photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. Plant Physiol 128:760–769

    Article  PubMed  CAS  Google Scholar 

  • Jones ML (2004) Changes in gene expression during senescence. In: Noodén LD (ed) Plant cell death processes. Elsevier, Amsterdam, pp 51–71

    Chapter  Google Scholar 

  • Kakizaki T, Matsumura H, Nakayama K, Che FS, Terauchi R, Inaba T (2009) Coordination of plastid protein import and nuclear gene expression by plastid-to-nucleus retrograde signaling. Plant Physiol 151:1339–1353

    Article  PubMed  CAS  Google Scholar 

  • Kane DJ, Sarafian TA, Anton R, Hahn H, Gralla EB, Valentine JS, Örd T, Bredesen DE (1993) Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science 262:1274–1277

    Article  PubMed  CAS  Google Scholar 

  • Kar M, Feierabend J (1984) Metabolism of activated oxygen in detached wheat and rye leaves and its relevance to the inhibition of senescence. Planta 160:385–391

    Article  CAS  Google Scholar 

  • Karpinski S, Wingsle G, Karpinska B, Hällgren JE (2001) Redox sensing of photooxidative stress and acclamatory mechanisms in plants. In: Aro EM, Andersson B (eds) Regulation of photosynthesis. Kluwer, Dordrecht, pp 469–486

    Google Scholar 

  • Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, Hwang D, Nam HG (2009) Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323:1053–1057

    Article  PubMed  CAS  Google Scholar 

  • Kotera E, Tasaka M, Shikanai T (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433:326–330

    Article  PubMed  CAS  Google Scholar 

  • Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–719

    Article  PubMed  CAS  Google Scholar 

  • Krause K, Krupinska K (2009) Nuclear regulators with a second home in organelles. Trends Plant Sci 14:194–199

    Article  PubMed  CAS  Google Scholar 

  • Külheim C, Ågren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93

    Article  PubMed  Google Scholar 

  • Kurepa J, Hérouart D, Van Montagu M, Inzé D (1997) Differential expression of CuZn- and Fe-superoxide dismutase genes of tobacco during development, oxidative stress and hormonal treatments. Plant Cell Physiol 38:463–470

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lascano HR, Casano LM, Martín M, Sabater B (2003) The activity of the chloroplastic Ndh complex is regulated by phosphorylation of the NDH-F subunit. Plant Physiol 132:256–262

    Article  PubMed  CAS  Google Scholar 

  • Leshem YY (1984) Interaction of cytokinins with lipid-associated oxy free radicals during senescence: a prospective mode of cytokinin action. Can J Bot 62:2943–2949

    Article  CAS  Google Scholar 

  • Leshem YY, Wurzburger J, Grossman S, Frimer AA (1981) Cytokinin interaction with free radical metabolism and senescence: effects of endogenous lipoxygenase and purine oxidation. Physiol Plant 53:9–12

    Article  CAS  Google Scholar 

  • Leshem YY, Halevy H, Frenkel C (1986) Processes and control of leaf senescence. Elsevier, Amsterdam

    Google Scholar 

  • Levine A (1999) Oxidative stress as a regulator of environmental responses in plants. In: Lerner HR (ed) Plant responses to environmental stress: from phytohormones to genome organization. Marcel Dekker, New York, pp 247–264

    Google Scholar 

  • Lezon TR, Banavar JR, Cieplak M, Maritan A, Fedoroff NV (2006) Using the principle of entropy maximization to infer genetic interaction networks from gene expression patterns. Proc Natl Acad Sci USA 103:19033–19038

    Article  PubMed  CAS  Google Scholar 

  • Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  PubMed  CAS  Google Scholar 

  • Liu L, Zhou Y, Zhou G, Ye R, Zhao L, Li X, Lin Y (2008) Identification of early senescence-associated genes in rice flag leaves. Plant Mol Biol 67:37–55

    Article  PubMed  CAS  Google Scholar 

  • Luquez VMC, Sasal Y, Medrano M, Martín MI, Mujica M, Guiamét JJ (2006) Quantitative trait loci analysis of leaf and plant longevity in Arabidopsis thaliana. J Exp Bot 57:1361–1372

    Article  CAS  Google Scholar 

  • Maier RM, Neckermann K, Igloi GL, Kössel H (1995) Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. J Mol Biol 251:614–628

    Article  PubMed  CAS  Google Scholar 

  • Mano J, Ohno C, Domac Y, Asada K (2001) Chloroplastic ascorbate peroxidase is the primary target of methylviologen-induced photooxidative stress in spinach leaves: its relevance to monodehydroascorbate radical detected with in vivo ESR. Biochim Biophys Acta 1504:275–287

    Article  PubMed  CAS  Google Scholar 

  • Maréchal A, Parent JS, Véronneau-Lafortune F, Jojeux A, Lang BF (2009) Whirly proteins maintain plastid genome stability in Arabidopsis. Proc Natl Acad Sci USA 106:14693–14698

    Article  PubMed  Google Scholar 

  • Martín M, Sabater B (2010) Plastid ndh genes in plant evolution. Plant Physiol Biochem 48:636–645

    Article  PubMed  CAS  Google Scholar 

  • Martín M, Casano LM, Sabater B (1996) Identification of the product of ndhA gene as a thylakoid protein synthesized in response to photooxidative treatment. Plant Cell Physiol 37:293–298

    Article  PubMed  Google Scholar 

  • Martín M, Casano LM, Zapata JM, Guéra A, del Campo EM, Schmitz-Linneweber C, Maier RM, Sabater B (2004) Role of thylakoid Ndh complex and peroxidase in the protection against photo-oxidative stress: fluorescence and enzyme activities in wild-type and ndhF-deficient tobacco. Physiol Plant 122:443–452

    Article  CAS  Google Scholar 

  • Martín M, Funk HT, Serrot PH, Poltnigg P, Sabater B (2009) Functional characterization of the thylakoid Ndh complex phosphorylation by site-directed mutations in the ndhF gene. Biochim Biophys Acta 1787:920–928

    Article  PubMed  CAS  Google Scholar 

  • Martínez P, López C, Roldán M, Sabater B, Martín M (1997) Plastid DNA of five ecotypes of Arabidopsis thaliana: sequence of the ndhG gene and maternal inheritance. Plant Sci 123:113–122

    Article  Google Scholar 

  • Matile P (2001) Senescence and cell death in plant development: chloroplast senescence and its regulation. In: Aro EM, Andersson B (eds) Regulation of photosynthesis. Kluwer, Dordrecht, pp 277–296

    Google Scholar 

  • McRae DG, Thompson JE (1983) Senescence-dependent changes in superoxide-anion production in illuminated chloroplasts from bean leaves. Planta 158:185–193

    Article  CAS  Google Scholar 

  • Mehta RA, Fawcett TW, Porath D, Matto AK (1992) Oxidative stress causes rapid membrane translocation and in vivo degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase. J Biol Chem 267:2810–2816

    PubMed  CAS  Google Scholar 

  • Mohapatra PK, Patro L, Raval MK, Biswal UC, Biswal B (2010) Senescence induced loss in photosynthesis enhances activity of cell wall β-glucosidase. Physiol Plant 138:346–355

    Article  PubMed  CAS  Google Scholar 

  • Monde RA, Greene JC, Stern DB (2000) The sequence and secondary structure of the 3′-UTR affect 3′-end maturation, RNA accumulation, and translation in tobacco chloroplasts. Plant Mol Biol 44:529–542

    Article  PubMed  CAS  Google Scholar 

  • Morgan PW, Drew MC (2004) Plant cell death and cell differentiation. In: Noodén LD (ed) Plant cell death processes. Elsevier, Amsterdam, pp 19–39

    Chapter  Google Scholar 

  • Morita K (1980) Release of nitrogen from chloroplasts during leaf senescence in rice (Oryza sativa L.). Ann Bot 46:297–302

    CAS  Google Scholar 

  • Muthuramalingam M, Seidel T, Laxa M, Nunes de Miranda SM, Gärtner F, Ströher E, Kandlbinder A, Dietz KJ (2009) Multiple redox and non-redox interactions define 2-Cys peroxiredoxin as a regulatory hub in the chloroplast. Mol Plant 2:1273–1288

    Article  PubMed  CAS  Google Scholar 

  • Nashilevitz S, Melamed-Bessudo C, Izkovich Y, Rogachev I, Osorio S, Itkin M, Adato A, Pankratov I, Hirschberg J, Fernie AR, Wolf S, Usadel B, Levy AA, Rumeau D, Aharoni A (2010) An orange ripening mutant links plastid NAD(P)H dehydrogenase complex activity to central and specialized metabolism during tomato fruit maturation. Plant Cell 22:1977–1997

    Article  PubMed  CAS  Google Scholar 

  • Nixon PJ, Rich PR (2007) Chlororespiratory pathways and their physiological significance. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, Berlin, pp 237–251

    Chapter  Google Scholar 

  • Noodén LD (ed) (2004) Plant cell death processes. Elsevier, Amsterdam

    Google Scholar 

  • Noodén LD, Guiamét JJ, Singh S, Letham DS, Tsuji J, Schneider MJ (1990) Hormonal control of senescence. In: Pharis RP, Rood SB (eds) Plant growth substances. Springer, Berlin, pp 537–546

    Google Scholar 

  • Ohad I, Vink M, Zer H, Herrman RG, Andersson B (2001) Novel aspect of the regulation of thylakoid protein phosphorylation. In: Aro EM, Andersson B (eds) Regulation of photosynthesis. Kluwer, Dordrecht, pp 419–432

    Google Scholar 

  • Ohe M, Rapolu M, Mieda T, Miyagawa Y, Yabuta Y, Yoshimura K, Shigeoka S (2005) Decline of leaf photooxidative stress tolerance with age in tobacco. Plant Sci 168:1487–1493

    Article  CAS  Google Scholar 

  • Okuda K, Chateigner-Boutin AL, Nakamura T, Delannoy E, Sugita M, Myouga F, Motohashi R, Shinozaki K, Small I, Shikanai T (2009) Pentatricopeptide repeat proteins with the DYW motif have distinct molecular functions in RNA editing and RNA cleavage in Arabidopsis chloroplasts. Plant Cell 21:146–156

    Article  PubMed  CAS  Google Scholar 

  • Orr WC, Sohal RS (1994) Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster. Science 263:1128–1130

    Article  PubMed  CAS  Google Scholar 

  • Osmond CB (1994) What is photoinhibition? Some insights from comparison of shade and sun plants. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis. BIOS Scientific, Oxford, pp 1–23

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pearcy RW (1994) Photosynthetic response to sunflecks and light gaps: mechanism and constrain. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis. BIOS Scientific, Oxford, pp 255–271

    Google Scholar 

  • Pich MM, Raule N, Catani L, Fagioli ME, Faenza I, Cocco L, Lenaz G (2004) Increased transcription of mitochondrial genes for complex I in human platelets during ageing. FEBS Lett 558:19–22

    Article  CAS  Google Scholar 

  • Piñas A, Strand Å (2008) Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Curr Opin Plant Biol 11:509–513

    Article  CAS  Google Scholar 

  • Potikha TS, Collins CC, Johnson DI, Delmer DP, Levine A (1999) The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol 119:849–858

    Article  PubMed  CAS  Google Scholar 

  • Prikryl J, Watkins KP, Friso G, Van Wijk KJ, Barkan A (2008) A member of the Whirly family is a multifunctional RNA- and DNA-binding protein that is essential for chloroplast biogenesis. Nucleic Acids Res 36:5152–5165

    Article  PubMed  CAS  Google Scholar 

  • Prochazkova D, Sairam RK, Srivastava GC, Singh DV (2001) Oxidative stress and antioxidant activity as the basis of senescence in maize. Plant Sci 161:765–771

    Article  CAS  Google Scholar 

  • Quarrie SA, Henson IE (1981) Abscisic acid accumulation in detached cereal leaves in response to water stress, II effect of leaf age and leaf position. Z Pflanzenphysiol 101:439–446

    CAS  Google Scholar 

  • Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5:278–282

    Article  PubMed  CAS  Google Scholar 

  • Reinbothe S, Reinbothe C, Parthier B (1993) Methyl jasmonate-regulated translation of nuclear encoded chloroplast protein in barley (Hordeum vulgare L. cv. Salome). J Biol Chem 268:10606–10611

    PubMed  CAS  Google Scholar 

  • Reyes JC, Muro-Pastor MI, Florencia FJ (2004) The GATA family of transcription factors in Arabidopsis and rice. Plant Physiol 134:1718–1732

    Article  PubMed  CAS  Google Scholar 

  • Rodermel S (2001) Pathways of plastid-to-nucleus signalling. Trends Plant Sci 6:471–478

    Article  PubMed  CAS  Google Scholar 

  • Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 30:1041–1051

    Article  PubMed  CAS  Google Scholar 

  • Sabater B (1985) Hormonal regulation of senescence. In: Purohit SS (ed) Hormonal regulation of plant growth and development. Kluwer, Dordrecht, pp 169–217

    Chapter  Google Scholar 

  • Samet JS, Sinclair TR (1980) Leaf senescence and abscisic acid in leaves of field-grown soybean. Plant Physiol 66:1164–1168

    Article  PubMed  CAS  Google Scholar 

  • Schaller F, Schalller A, Stintzi A (2005) Biosynthesis and metabolism of jasmonates. J Plant Growth Regul 23:179–199

    Google Scholar 

  • Schommer C, Palatnik JF, Aggarwal P, Chételat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6:e230

    Article  PubMed  CAS  Google Scholar 

  • Seltmann MA, Stingl NE, Lautenschlaeger JK, Krischke M, Mueller MJ, Berger S (2010) Differential impact of lipoxygenase 2 and jasmonates on natural and stress-induced senescence in Arabidopsis. Plant Physiol 152:1940–1950

    Article  PubMed  CAS  Google Scholar 

  • Serrot PH, Sabater B, Martín M (2008) Expression of the ndhCKJ operon of barley and editing at the 13th base of the mRNA of the ndhC gene. Biol Plant 52:347–350

    Article  CAS  Google Scholar 

  • Singh KB, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  PubMed  CAS  Google Scholar 

  • Smart C (1994) Gene expression during leaf senescence. New Phytol 126:419–448

    Article  CAS  Google Scholar 

  • Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065

    Article  PubMed  CAS  Google Scholar 

  • Thimann KV (1978) The senescence of leaves. What’s New Plant Physiol 9:9–12

    Google Scholar 

  • Thomas H, Stoddart JL (1980) Leaf senescence. Annu Rev Plant Physiol 31:83–111

    Article  CAS  Google Scholar 

  • Thomas H, Huang L, Young M, Ougham H (2009) Evolution of plant senescence. BMC Evol Biol 9:163–196

    Article  PubMed  CAS  Google Scholar 

  • Thompson WW, Legge RL, Barber RF (1987) The role of free radicals in senescence and wounding. New Phytol 105:317–344

    Article  CAS  Google Scholar 

  • Tillich M, Funk HT, Schmitz-Linneweber C, Poltnigg P, Sabater B, Martin M, Maier RM (2005) Editing of plastid RNA in Arabidopsis thaliana ecotypes. Plant J 43:708–715

    Article  PubMed  CAS  Google Scholar 

  • Tomás R, Vera A, Martín M, Sabater B (1992) Changes in protein synthesis without evidence of DNA methylation in barley chloroplasts during leaf growth and development. Plant Sci 85:71–77

    Article  Google Scholar 

  • Vailleau F, Daniel X, Tronchet M, Montillet JL, Triantaphylides C, Roby D (2002) A R2R3-MYB gene, AtMYB30, acts as a positive regulator of the hypersensitive cell death program in plants in response to pathogen attack. Proc Natl Acad Sci USA 99:10179–10184

    Article  PubMed  CAS  Google Scholar 

  • Van Breusegem F, Vranová E, Dat JF, Inzé D (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161:405–414

    Article  Google Scholar 

  • Van Doorn WG, Yoshimoto K (2010) Role of chloroplasts and other plastids in ageing and death of plants and animals: a tale of Vishnu and Shiva. Ageing Res Rev 9:117–130

    Article  PubMed  Google Scholar 

  • Vera A, Tomás R, Martín M, Sabater B (1990) Apparent expression of small single copy cpDNA region in senescent chloroplasts. Plant Sci 72:63–67

    Article  CAS  Google Scholar 

  • Von Gromoff ED, Schroda M, Oster U, Beck CF (2006) Identification of a plastid response element that acts as an enhancer within the Chlamydomonas HSP70A promoter. Nucleic Acids Res 34:4767–4779

    Article  CAS  Google Scholar 

  • Wagner D, Przybyla D, op den Camp R, Kim C, Landgraf F, Lee KP, Würsch M, Laloi C, Nater M, Hideg E, Apel K (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183–1185

    Article  PubMed  CAS  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  PubMed  CAS  Google Scholar 

  • Woo HA, Yim SH, Shin DH, Kang D, Yu DY, Rhee SG (2010) Inactivation of peroxiredoxin I by phosphorylation allows localized H2O2 accumulation for cell signaling. Cell 140:517–528

    Article  PubMed  CAS  Google Scholar 

  • Woolhouse HW (1984) The biochemistry and regulation of senescence in chloroplasts. Can J Bot 62:2934–2941

    Article  CAS  Google Scholar 

  • Wright H, Van Doorn WG, Gunawardena A (2009) In vivo study of developmental programmed cell death using the lace plant (Aponogeton madagascariensis; Aponogetonaceae) leaf model system. Am J Bot 96:865–876

    Article  PubMed  Google Scholar 

  • Yao N, Greenberg JT (2006) Arabidopsis accelerated cell death2(?) modulates programmed cell death. Plant Cell 18:397–411

    Article  PubMed  CAS  Google Scholar 

  • Yen CH, Yang CH (1998) Evidence for programmed cell death during leaf senescence in plants. Plant Cell Physiol 39:922–927

    Article  CAS  Google Scholar 

  • Zapata JM, Guéra A, Esteban-Carrasco A, Martín M, Sabater B (2005) Chloroplasts regulate leaf senescence: delayed senescence in transgenic ndhF-defective tobacco. Cell Death Differ 12:1277–1284

    Article  PubMed  CAS  Google Scholar 

  • Zentgraf U (2007) Oxidative stress abd leaf senescence. In: Gan S (ed) Senescence processes in plants. Blackwell, Oxford, pp 69–86

    Chapter  Google Scholar 

  • Zhou DX (1999) Regulatory mechanism of plant gene transcription by GT-elements and GT-factors. Trends Plant Sci 4:210–214

    Article  PubMed  Google Scholar 

  • Zimmermann P, Zentgraf U (2005) The correlation between oxidative stress and leaf senescence during plant leaf development. Cell Mol Biol Lett 10:515–534

    PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Patricia H. Serrot for stimulating discussions and English corrections. Research support was provided by Spanish MCYT.

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  1. Department of Plant Biology, University of Alcalá, Alcalá de Henares, 28871, Madrid, Spain

    Bartolomé Sabater & Mercedes Martín

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  1. Bartolomé Sabater
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  2. Mercedes Martín
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Correspondence to Bartolomé Sabater .

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  1. , School of Life Sciences, Sambalpur University, Jyotivihar, Sambalpur, 768019, Orissa, India

    Basanti Biswal

  2. Botanisches Institut, Universität Kiel, Olshausenstr. 40, Kiel, 24118, Germany

    Karin Krupinska

  3. School of Life Sciences, Sambalpur University, Orissa, 768 019, India

    Udaya C. Biswal

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Sabater, B., Martín, M. (2013). Chloroplast Control of Leaf Senescence. In: Biswal, B., Krupinska, K., Biswal, U. (eds) Plastid Development in Leaves during Growth and Senescence. Advances in Photosynthesis and Respiration, vol 36. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5724-0_23

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