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Plastid Signaling During the Plant Life Cycle

Plastid Function as Developmental Reporter and Environmental Sensor in Plant Growth and Acclimation

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Plastid Development in Leaves during Growth and Senescence

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

Summary

Plastids are semi-autonomous organelles of endosymbiotic origin. They possess their own DNA and a complete machinery to express the encoded information on it. However, the genome size is limited to about 120 genes encoding mainly components of the gene expression and photosynthesis machineries. For complete functionality, therefore, plastids largely depend on the import of cytosolic proteins since all plastid protein complexes are comprised of a mosaic of plastid and nuclear encoded components. Proper development and function of plastids, thus, requires a tight coordination of gene expression in the genetic compartments of a plant cell. This coordination is obtained by (1) nucleus-to-plastid signals which guarantee an appropriate establishment of the plastid type according to the tissues context of the plant cell, and by (2) plastid-to-nucleus signals which report the actual developmental and functional stage of the plastids to the nucleus. This mutual communication controls the expression of appropriate genes providing the right gene products required for the respective condition. Plastidial signals can be distinguished into distinct classes covering signals from (1) plastid gene expression, (2) pigment biosynthesis pathways, (3) pools of reactive oxygen species, (4) redox states of photosynthetic components and (5) metabolic intermediates such as sugars. This classification is mainly focused on the experimental system in which the respective plastid signal has been analyzed rather than describing the signal itself. In this review we follow a different strategy and summarize the current knowledge on plastid signaling according to the developmental stage of the plastids. We distinguish between signals from early plastid development, from mature plastids and from plastids being degraded during senescence. This also includes the action of three important plant hormones synthesized partly in the plastids, jasmonic acid, salicylic acid and abscisic acid. By this way we follow the plant’s life cycle and put the roles of plastidial signals into a functional and developmental context which provides novel insights into the fascinating research field of intracellular signaling.

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Abbreviations

ABA:

Abscisic acid;

ALA:

Amino levulinic acid;

GSH:

Reduced glutathione;

JA:

Jasmonic acid;

Mg-proto-IX:

Magnesium-protoporphyrin IX;

NF:

Norflurazon;

ROS:

Reactive oxygen species;

SA:

Salicylic acid

References

  • Abdallah F, Salamini F, Leister D (2000) A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends Plant Sci 5:141–142

    Article  PubMed  CAS  Google Scholar 

  • Abreu ME, Munné-Bosch S (2009) Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana. J Exp Bot 60:1261–1271

    Article  PubMed  CAS  Google Scholar 

  • Acevedo-Hernández GJ, León P, Herrera-Estrella LR (2005) Sugar and ABA responsiveness of a minimal RBCS light-responsive unit is mediated by direct binding of ABI4. Plant J 43:506–519

    Article  PubMed  CAS  Google Scholar 

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  PubMed  CAS  Google Scholar 

  • Albrecht V, Ingenfeld A, Apel K (2006) Characterization of the snowy cotyledon 1 mutant of Arabidopsis thaliana: the impact of chloroplast elongation factor G on chloroplast development and plant vitality. Plant Mol Biol 60:507–518

    Article  PubMed  CAS  Google Scholar 

  • Allen JF, Raven JA (1996) Free-radical-induced mutation vs redox regulation: costs and benefits of genes in organelles. J Mol Evol 42:482–492

    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 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Arsova B, Hoja U, Wimmelbacher M, Greiner E, Ustun S, Melzer M, Petersen K, Lein W, Bornke F (2010) Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell 22:1498–1515

    Article  PubMed  CAS  Google Scholar 

  • Asensi-Fabado MA, Munné-Bosch S (2011) The aba3-1 mutant of Arabidopsis thaliana withstands moderate doses of salt stress by modulating leaf growth and salicylic acid levels. J Plant Growth Regul 30:456–466

    Article  CAS  Google Scholar 

  • Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321

    Article  PubMed  CAS  Google Scholar 

  • Baier M, Dietz KJ (2005) Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology. J Exp Bot 56:1449–1462

    Article  PubMed  CAS  Google Scholar 

  • Ball L, Accotto GP, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM (2004) Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16:2448–2462

    Article  PubMed  CAS  Google Scholar 

  • Beck CF (2001) Signaling pathways in chloroplast-to-nucleus communication. Protist 152:175–182

    Article  PubMed  CAS  Google Scholar 

  • Beck CF (2005) Signaling pathways from the chloroplast to the nucleus. Planta 222:743–756

    Article  PubMed  CAS  Google Scholar 

  • Blomqvist LA, Ryberg M, Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals their significance in chloroplast development. Photosynth Res 96:37–50

    Article  PubMed  CAS  Google Scholar 

  • Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, Jahns P, Leister D (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437:1179–1182

    Article  PubMed  CAS  Google Scholar 

  • Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8:443–449

    Article  PubMed  CAS  Google Scholar 

  • Bouwmeester HJ, Roux C, López Ráez JA, Bécard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230

    Article  PubMed  CAS  Google Scholar 

  • Bradbeer JW, Atkinson YE, Börner T, Hagemann R (1979) Cytoplasmic synthesis of plastid polypeptides may be controlled by plastid synthesized RNA. Nature 279:816–817

    Article  CAS  Google Scholar 

  • Bräutigam K, Dietzel L, Pfannschmidt T (2007) Plastid-nucleus communication: anterograde and retrograde signalling in development and function of plastids. In: Bock R (ed) Cell and molecular biology of plastids, vol 19, Topics in current genetics. Springer, Berlin, pp 409–455

    Chapter  Google Scholar 

  • Bräutigam K, Dietzel L, Kleine T, Ströher E, Wormuth D, Dietz KJ, Radke D, Wirtz M, Hell R, Dörmann P, Nunes-Nesi A, Schauer N, Fernie AR, Oliver SN, Geigenberger P, Leister D, Pfannschmidt T (2009) Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis. Plant Cell 21:2715–2732

    Article  PubMed  Google Scholar 

  • Bräutigam K, Dietzel L, Pfannschmidt T (2010) Hypothesis – a binary redox control mode as universal regulator of photosynthetic light acclimation. Plant Signal Behav 5:81–85

    Article  PubMed  Google Scholar 

  • Buchanan BB, Gruissem W, Jones RL (2002) Biochemistry and molecular biology of plants. Wiley, Somerset

    Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver CJ (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 

  • Burbidge A, Grieve TM, Jackson A, Thompson A, McCarty DR, Taylor IB (1999) Characterization of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J 17:427–431

    Article  PubMed  CAS  Google Scholar 

  • Cazzonelli CI (2011) Carotenoids in nature: insights from plants and beyond. Funct Plant Biol 38:833–847

    Article  CAS  Google Scholar 

  • Cazzonelli CI, Yin K, Pogson BJ (2009) Potential implications for epigenetic regulation of carotenoid biosynthesis during root and shoot development. Plant Signal Behav 4:339–341

    Article  PubMed  CAS  Google Scholar 

  • Cazzonelli CI, Roberts AC, Carmody ME, Pogson BJ (2010) Transcriptional control of SET DOMAIN GROUP 8 and CAROTENOID ISOMERASE during Arabidopsis development. Mol Plant 3:174–191

    Article  PubMed  CAS  Google Scholar 

  • Chamovitz D, Pecker I, Hirschberg J (1991) The molecular basis of resistance to the herbicide norflurazon. Plant Mol Biol 16:967–974

    Article  PubMed  CAS  Google Scholar 

  • Chandok MR, Sopory SK, Oelmüller R (2001) Cytoplasmic kinase and phosphatase activities can induce PsaF gene expression in the absence of functional plastids: evidence that phosphorylation/dephosphorylation events are involved in interorganellar crosstalk. Mol Gen Genet 264:819–826

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Gong Z, Zhu JK (2008) Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Integr Plant Biol 50:1187–1195

    Article  PubMed  CAS  Google Scholar 

  • Christmann A, Hoffmann T, Teplova I, Grill E, Müller A (2005) Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis. Plant Physiol 137:209–219

    Article  PubMed  CAS  Google Scholar 

  • Dangl JL, Dietrich RA, Thomas H (2000) Senescence and programmed cell death. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. ASPB, Rockville, pp 1044–1100

    Google Scholar 

  • Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268–281

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (2000) Photosynthesis – harvesting sunlight safely. Nature 403:373–374

    Article  Google Scholar 

  • Desikan R, Mackerness SAH, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172

    Article  PubMed  CAS  Google Scholar 

  • Durnford DG, Falkowski PG (1997) Chloroplast redox regulation of nuclear gene transcription during photoacclimation. Photosynth Res 53:229–241

    Article  CAS  Google Scholar 

  • Enami K, Ozawa T, Motohashi N, Nakamura M, Tanaka K, Hanaoka M (2011) Plastid-to-nucleus retrograde signals are essential for the expression of nuclear starch biosynthesis genes during amyloplast differentiation in tobacco BY-2 cultured cells. Plant Physiol 157:518–530

    Article  PubMed  CAS  Google Scholar 

  • Escoubas JM, Lomas M, Laroche J, Falkowski PG (1995) Light-intensity regulation of cab gene-transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA 92:10237–10241

    Article  PubMed  CAS  Google Scholar 

  • Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D, Carrie C, Giraud E, Whelan J, David P, Javot H, Brearley C, Hell R, Marin E, Pogson BJ (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012

    Article  PubMed  CAS  Google Scholar 

  • Fey V, Wagner R, Brautigam K, Wirtz M, Hell R, Dietzmann A, Leister D, Oelmüller R, Pfannschmidt T (2005) Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J Biol Chem 280:5318–5328

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    Article  PubMed  CAS  Google Scholar 

  • Frechilla S, Talbott LD, Bogomolni RA, Zeiger E (2000) Reversal of blue light-stimulated stomatal opening by green light. Plant Cell Physiol 41:171–176

    Article  PubMed  CAS  Google Scholar 

  • Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33:691–705

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Giuliano G, Al-Babili S, von Lintig J (2003) Carotenoid oxygenases: cleave it or leave it. Trends Plant Sci 8:145–149

    Article  PubMed  CAS  Google Scholar 

  • Gómez-Roldán V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194

    Article  PubMed  CAS  Google Scholar 

  • Gray JC, Sornarajah R, Zabron AA, Duckett CM, Khan MS (1995) Chloroplast control of nuclear gene expression. Photosynthesis, from light to biosphere. Kluwer, Dordrecht

    Google Scholar 

  • Gray JC, Sullivan JA, Wang JH, Jerome CA, MacLean D (2003) Coordination of plastid and nuclear gene expression. Philos T Roy Soc B 358:135–144

    Article  CAS  Google Scholar 

  • Hanaoka M, Kanamaru K, Takahashi H, Tanaka K (2003) Molecular genetic analysis of chloroplast gene promoters dependent on SIG2, a nucleus-encoded sigma factor for the plastid-encoded RNA polymerase, in Arabidopsis thaliana. Nucleic Acids Res 31:7090–7098

    Article  PubMed  CAS  Google Scholar 

  • He YH, Tang W, Swain JD, Green AL, Jack TP, Gan S (2001) Networking senescence-regulating pathways by using Arabidopsis enhancer trap lines. Plant Physiol 126:707–713

    Article  PubMed  CAS  Google Scholar 

  • He YH, Fukushige H, Hildebrand DF, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128:876–884

    Article  PubMed  CAS  Google Scholar 

  • Heiber I, Stroher E, Raatz B, Busse I, Kahmann U, Bevan MW, Dietz KJ, Baier M (2007) The redox imbalanced mutants of Arabidopsis differentiate signaling pathways for redox regulation of chloroplast antioxidant enzymes. Plant Physiol 143:1774–1788

    Article  PubMed  CAS  Google Scholar 

  • Hoober JK (2006) Chloroplast development: whence and whither. In: Wise RR, Hoober JK (eds) The structure and function of plastids, vol 23. Springer, Dordrecht, pp 27–51

    Chapter  Google Scholar 

  • Hörtensteiner S, Kräutler B (2011) Chlorophyll breakdown in higher plants. Biochim Biophys Acta 1807:977–988

    Article  PubMed  CAS  Google Scholar 

  • Isemer R, Mulisch M, Schäfer A, Kirchner S, Koop H-U, Krupinska K (2012) Plastid encoded Whirly 1 is translocated to the nucleus. FEBS Lett 586:85–88

    Article  PubMed  CAS  Google Scholar 

  • Jarvis P (2007) Intracellular signalling: chloroplast backchat. Curr Biol 17:R552–R555

    Article  PubMed  CAS  Google Scholar 

  • Johanningmeier U, Howell SH (1984) Regulation of light-harvesting chlorophyll-binding protein messenger-RNA accumulation in Chlamydomonas reinhardtii – possible involvement of chlorophyll synthesis precursors. J Biol Chem 259:3541–3549

    Google Scholar 

  • Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9:627–640

    PubMed  CAS  Google Scholar 

  • Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657

    Article  PubMed  CAS  Google Scholar 

  • Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjolander K, Gruissem W, Baginsky S (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr Biol 14:354–362

    Article  PubMed  CAS  Google Scholar 

  • Kleine T, Voigt C, Leister D (2009) Plastid signalling to the nucleus: messengers still lost in the mists? Trends Genet 25:185–190

    Article  PubMed  CAS  Google Scholar 

  • Koncz C, Mayerhofer R, Konczkalman Z, Nawrath C, Reiss B, Redei GP, Schell J (1990) Isolation of a gene encoding a novel chloroplast protein by T-DNA tagging in Arabidopsis thaliana. EMBO J 9:1337–1346

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940–2945

    Article  PubMed  CAS  Google Scholar 

  • Kropat J, Oster U, Rudiger W, Beck CF (1997) Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proc Natl Acad Sci USA 94:14168–14172

    Article  PubMed  CAS  Google Scholar 

  • Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299:902–906

    Article  PubMed  CAS  Google Scholar 

  • 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 Natl Acad Sci USA 104:10270–10275

    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 

  • Lonosky PM, Zhang XS, Honavar VG, Dobbs DL, Fu A, Rodermel SR (2004) A proteomic analysis of maize chloroplast biogenesis. Plant Physiol 134:560–574

    Article  PubMed  CAS  Google Scholar 

  • López Ráez JA, Bouwmeester H (2008) Fine-tuning regulation of strigolactone biosynthesis under phosphate starvation. Plant Signal Behav 3:963–965

    PubMed  Google Scholar 

  • Lopez-Juez E, Pyke KA (2005) Plastids unleashed: their development and their integration in plant development. Int J Dev Biol 49:557–577

    Article  PubMed  CAS  Google Scholar 

  • López Ráez JA, Charnikhova T, Gómez Roldán V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech Pages V, Bécard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874

    Article  PubMed  CAS  Google Scholar 

  • Lukens JH, Mathews DE, Durbin RD (1987) Effect of tagetitoxin on the levels of ribulose 1,5-bisphosphate carboxylase, ribosomes, and RNA in plastids of wheat leaves. Plant Physiol 84:808–813

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99:12246–12251

    Article  PubMed  CAS  Google Scholar 

  • Matusova R, Rani K, Verstappen FWA, Franssen MCR, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934

    Article  PubMed  CAS  Google Scholar 

  • Maxwell DP, Laudenbach DE, Huner NPA (1995) Redox regulation of light-harvesting complex-II and cab messenger-RNA abundance in Dunaliella salina. Plant Physiol 109:787–795

    PubMed  CAS  Google Scholar 

  • Mayfield SP, Taylor WC (1984) Carotenoid-deficient maize seedlings fail to accumulate light-harvesting chlorophyll a/b binding-protein (Lhcb) messenger-RNA. Eur J Biochem 144:79–84

    Article  PubMed  CAS  Google Scholar 

  • Mayfield SP, Nelson T, Taylor WC (1986) The fate of chloroplast proteins during photooxidation in carotenoid-deficient maize leaves. Plant Physiol 82:760–764

    Article  PubMed  CAS  Google Scholar 

  • McCourt P, Creelman R (2008) The ABA receptor – we report you decide. Curr Opin Plant Biol 11:474–478

    Article  PubMed  CAS  Google Scholar 

  • Meskauskiene R, Nater M, Goslings D, Kessler F, den Camp RO, Apel K (2001) FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 98:12826–12831

    Article  PubMed  CAS  Google Scholar 

  • Métraux JP (2002) Recent breakthroughs in the study of salicylic acid biosynthesis. Trends Plant Sci 7:332–334

    Article  PubMed  Google Scholar 

  • Milanowska J, Gruczecki W (2005) Heat-induced and light-induced isomerization of the xanthophyll pigment zeaxanthin. J Photochem Photobiol B Biol 80:178–186

    Article  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Lee J, Miura T, Hasegawa P (2010) SIZ1 controls cell growth and plant development in Arabidopsis through salicylic acid. Plant Cell Physiol 51:103–113

    Article  PubMed  CAS  Google Scholar 

  • Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA 98:2053–2058

    Article  PubMed  CAS  Google Scholar 

  • Mochizuki N, Tanaka R, Tanaka A, Masuda T, Nagatani A (2008) The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis. Proc Natl Acad Sci USA 105:15184–15189

    Article  PubMed  CAS  Google Scholar 

  • Morris K, AH-Mackerness S, Page T, John CF, Murphy AM, Carr JP, Buchanan-Wollaston V (2000) Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J 23:677–685

    Article  PubMed  CAS  Google Scholar 

  • Motohashi R, Yamazaki T, Myouga F, Ito T, Ito K, Satou M, Kobayashi M, Nagata N, Yoshida S, Nagashima A, Tanaka K, Takahashi S, Shinozaki K (2007) Chloroplast ribosome release factor 1 (AtcpRF1) is essential for chloroplast development. Plant Mol Biol 64:481–497

    Article  PubMed  CAS  Google Scholar 

  • Moulin M, McCormac AC, Terry MJ, Smith AC (2008) Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc Natl Acad Sci USA 105:15178–15183

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mullineaux PM, Rausch T (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynth Res 86:459–474

    Article  PubMed  CAS  Google Scholar 

  • Munné-Bosch S (2008) Do perennials really senesce? Trends Plant Sci 13:216–220

    Article  PubMed  CAS  Google Scholar 

  • Munné-Bosch S, Alegre L (2002) The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21:31–57

    Google Scholar 

  • Munné-Bosch S, Alegre L (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Funct Plant Biol 31:203–213

    Article  Google Scholar 

  • Mur LA, Aubry S, Mondhe M, Kingston-Smith A, Gallagher J, Timms-Taravella E, James C, Papp I, Hörtensteiner S, Thomas H, Ougham H (2010) Accumulation of chlorophyll catabolites photosensitizes the hypersensitive response elicited by Pseudomonas syringae in Arabidopsis. New Phytol 188:161–174

    Article  PubMed  CAS  Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    Article  PubMed  CAS  Google Scholar 

  • Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460

    Article  PubMed  CAS  Google Scholar 

  • Noctor G, Veljovic-Jovanovic S, Foyer CH (2000) Peroxide processing in photosynthesis: antioxidant coupling and redox signalling. Philos T Roy Soc B 355:1465–1475

    Article  CAS  Google Scholar 

  • Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57:739–759

    Article  PubMed  CAS  Google Scholar 

  • Oelmüller R (1989) Photooxidative destruction of chloroplasts and its effect on nuclear gene-expression and extraplastidic enzyme levels. Photochem Photobiol 49:229–239

    Article  Google Scholar 

  • Oelmüller R, Mohr H (1986) Photooxidative destruction of chloroplasts and its consequences for expression of nuclear genes. Planta 167:106–113

    Article  Google Scholar 

  • Oelmüller R, Levitan I, Bergfeld R, Rajasekhar VK, Mohr H (1986) Expression of nuclear genes as affected by treatments acting on the plastids. Planta 168:482–492

    Article  Google Scholar 

  • op den Camp RGL, Przybyla D, Ochsenbein C, Laloi C, Kim CH, Danon A, Wagner D, Hideg E, Gobel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332

    Article  PubMed  CAS  Google Scholar 

  • Oswald O, Martin T, Dominy PJ, Graham IA (2001) Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc Natl Acad Sci USA 98:2047–2052

    Article  PubMed  CAS  Google Scholar 

  • Paolicchi F, Lombardi L, Ceccarelli N, Lorenzi R (2005) Are retinal and retinal-binding proteins involved in stomatal response to blue light? Funct Plant Biol 32:1135–1141

    Article  CAS  Google Scholar 

  • Papenbrock J, Grimm B (2001) Regulatory network of tetrapyrrole biosynthesis – studies of intracellular signalling involved in metabolic and developmental control of plastids. Planta 213:667–681

    Article  PubMed  CAS  Google Scholar 

  • Parvathi K, Raghavendra AS (1997) Blue light-promoted stomatal opening in abaxial epidermis of Commelina benghalensis is maximal at low calcium. Physiol Plant 101:861–864

    Article  CAS  Google Scholar 

  • Pei ZM, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734

    Article  PubMed  CAS  Google Scholar 

  • Pesaresi P, Masiero S, Eubel H, Braun HP, Bhushan S, Glaser E, Salamini F, Leister D (2006) Nuclear photosynthetic gene expression is synergistically modulated by rates of protein synthesis in chloroplasts and mitochondria. Plant Cell 18:970–991

    Article  PubMed  CAS  Google Scholar 

  • Pesaresi P, Schneider A, Kleine T, Leister D (2007) Interorganellar communication. Curr Opin Plant Biol 10:600–606

    Article  PubMed  CAS  Google Scholar 

  • Pesaresi P, Hertle A, Pribil M, Kleine T, Wagner R, Strissel H, Ihnatowicz A, Bonardi V, Scharfenberg M, Schneider A, Pfannschmidt T, Leister D (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21:2402–2423

    Article  PubMed  CAS  Google Scholar 

  • Petracek ME, Dickey LF, Huber SC, Thompson WF (1997) Light-regulated changes in abundance and polyribosome association of ferredoxin mRNA are dependent on photosynthesis. Plant Cell 9:2291–2300

    PubMed  CAS  Google Scholar 

  • Petracek ME, Dickey LF, Nguyen TT, Gatz C, Sowinski DA, Allen GC, Thompson WF (1998) Ferredoxin-1 mRNA is destabilized by changes in photosynthetic electron transport. Proc Natl Acad Sci USA 95:9009–9013

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8:33–41

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T (2010) Plastidial retrograde signalling – a true “plastid factor” or just metabolite signatures? Trends Plant Sci 15:427–435

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T, Link G (1997) The A and B forms of plastid DNA-dependent RNA polymerase from mustard (Sinapis alba L.) transcribe the same genes in a different developmental context. Mol Gen Genet 257:35–44

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T, Schutze K, Brost M, Oelmüller R (2001) A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. J Biol Chem 276:36125–36130

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T, Schutze K, Fey V, Sherameti I, Oelmüller R (2003) Chloroplast redox control of nuclear gene expression – a new class of plastid signals in interorganellar communication. Antioxid Redox Signal 5:95–101

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T, Brautigam K, Wagner R, Dietzel L, Schroter Y, Steiner S, Nykytenko A (2009) Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding. Ann Bot 103:599–607

    Article  PubMed  CAS  Google Scholar 

  • Piippo M, Allahverdiyeva Y, Paakkarinen V, Suoranta UM, Battchikova N, Aro EM (2006) Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. Physiol Genomics 25:142–152

    Article  PubMed  CAS  Google Scholar 

  • Pogson BJ, Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development: an overview. Plant Physiol 155:1545–1551

    Article  PubMed  CAS  Google Scholar 

  • Pogson BJ, Woo NS, Förster B, Small ID (2008) Plastid signalling to the nucleus and beyond. Trends Plant Sci 13:602–609

    Article  PubMed  CAS  Google Scholar 

  • Pursiheimo S, Mulo P, Rintamaki E, Aro EM (2001) Coregulation of light-harvesting complex II phosphorylation and Lhcb mRNA accumulation in winter rye. Plant J 26:317–327

    Article  PubMed  CAS  Google Scholar 

  • Rani K, Zwanenburg B, Sugimoto Y, Yoneyama K, Bouwmeester HJ (2008) Biosynthetic considerations could assist the structure elucidation of host plant produced rhizosphere signalling compounds (strigolactones) for arbuscular mycorrhizal fungi and parasitic plants. Plant Physiol Biochem 46:617–626

    Article  PubMed  CAS  Google Scholar 

  • Rapp JC, Mullet JE (1991) Chloroplast transcription is required to express the nuclear genes RbcS and Cab. Plastid DNA copy number is regulated independently. Plant Mol Biol 17:813–823

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rüdiger W, Grimm B (2006) Chlorophyll metabolism, an overview. In: Grimm B, Porra RJ, Rüdiger W, Scheer H (eds) Advances in photosynthesis and respiration. Springer, Dordrecht, pp 133–146

    Google Scholar 

  • Schaller F (2001) Enzymes of the biosynthesis of octadecanoid-derived signaling molecules. J Exp Bot 52:11–23

    Article  PubMed  CAS  Google Scholar 

  • Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874

    Article  PubMed  CAS  Google Scholar 

  • Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7:41–48

    Article  PubMed  CAS  Google Scholar 

  • Shang Y, Yan L, Liu ZQ, Cao Z, Mei C, Xin Q, Wu FQ, Wang XF, Du SY, Jiang T, Zhang XF, Zhao R, Sun HL, Liu R, Yu YT, Zhang DP (2010) The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22:1909–1935

    Article  PubMed  CAS  Google Scholar 

  • Shen Y-Y, Wang X-F, Wu F-O, Du S-Y, Cao Z, Shang Y, Wang X-L, Peng C-C, Yu X-C, Zhu S-Y, Fan R-C, Xu Y-H, Zhang D-P (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823–826

    Article  PubMed  CAS  Google Scholar 

  • Sherameti I, Nakamura M, Yamamoto YY, Pfannschmidt T, Obokata J, Oelmüller R (2002a) Polyribosome loading of spinach mRNAs for photosystem I subunits is controlled by photosynthetic electron transport – a crucial cis element in the spinach PsaD gene is located in the 5′-untranslated region. Plant J 32:631–639

    Article  PubMed  CAS  Google Scholar 

  • Sherameti I, Sopory SK, Trebicka A, Pfannschmidt T, Oelmüller R (2002b) Photosynthetic electron transport determines nitrate reductase gene expression and activity in higher plants. J Biol Chem 277:46594–46600

    Article  PubMed  CAS  Google Scholar 

  • Smart CM (1994) Gene expression during leaf senescence. New Phytol 126:418–449

    Article  Google Scholar 

  • Steiner S, Schröter Y, Pfalz J, Pfannschmidt T (2011) Identification of essential subunits in the plastid-encoded RNA polymerase complex reveals building blocks for proper plastid development. Plant Physiol 157:1–13

    Article  CAS  Google Scholar 

  • Stoebe B, Maier UG (2002) One, two, three: nature’s tool box for building plastids. Protoplasma 219:123–130

    Article  PubMed  Google Scholar 

  • Strand A (2004) Plastid-to-nucleus signalling. Curr Opin Plant Biol 7:621–625

    Article  PubMed  CAS  Google Scholar 

  • Strand A, Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421:79–83

    Article  PubMed  CAS  Google Scholar 

  • Strand A, Kleine T, Chory J (2006) Plastid-to-nucleus signaling. In: Wise RR, Hoober JK (eds) The structure and function of plastids, vol 23. Springer, Dordrecht, pp 183–197

    Chapter  Google Scholar 

  • Sugiura M (1992) The chloroplast genome. Plant Mol Biol 19:149–168

    Article  PubMed  CAS  Google Scholar 

  • Sullivan JA, Gray JC (1999) Plastid translation is required for the expression of nuclear photosynthesis genes in the dark and in roots of the pea lip1 mutant. Plant Cell 11:901–910

    PubMed  CAS  Google Scholar 

  • Sullivan JA, Gray JC (2002) Multiple plastid signals regulate the expression of the pea plastocyanin gene in pea and transgenic tobacco plants. Plant J 32:763–774

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Feng P, Xu X, Guo H, Ma J, Chi W, Lin R, Lu C, Zhang L (2011) A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nat Commun 2:477

    Google Scholar 

  • Surpin M, Larkin RM, Chory J (2002) Signal transduction between the chloroplast and the nucleus. Plant Cell 14:S327–S338

    PubMed  CAS  Google Scholar 

  • Susek RE, Ausubel FM, Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear Cab and RbcS gene-expression from chloroplast development. Cell 74:787–799

    Article  PubMed  CAS  Google Scholar 

  • Talbot LD, Hammad JW, Harn LC, Nguyen VH, Patel J, Zeiger E (2006) Reversal by green light of blue light-stimulated stomatal opening in intact, attached leaves of Arabidopsis operates only in the potassium-dependent, morning phase of movement. Plant Cell Physiol 47:332–339

    Article  CAS  Google Scholar 

  • Tan BC, Schwartz SH, Zeevaart JA, McCarty DR (1997) Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA 94:12235–12240

    Article  PubMed  CAS  Google Scholar 

  • Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346

    Article  PubMed  CAS  Google Scholar 

  • Taylor WC (1989) Regulatory interactions between nuclear and plastid genomes. Annu Rev Plant Physiol 40:211–233

    CAS  Google Scholar 

  • Tikkanen M, Piippo M, Suorsa M, Sirpio S, Mulo P, Vainonen J, Vener AV, Allahverdiyeva Y, Aro EM (2006) State transitions revisited – a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol Biol 62:779–793

    Article  PubMed  CAS  Google Scholar 

  • Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135

    Article  PubMed  CAS  Google Scholar 

  • Tottey S, Block MA, Allen M, Westergren T, Albrieux C, Scheller HV, Merchant S, Jensen PE (2003) Arabidopsis CHL27, located in both envelope and thylakoid membranes, is required for the synthesis of protochlorophyllide. Proc Natl Acad Sci USA 100:16119–16124

    Article  PubMed  CAS  Google Scholar 

  • Tsuzuki T, Takahashi K, Inoue S, Okigaki Y, Tomiyama M, Hossain MA, Shimazaki K, Murata Y, Kinoshita T (2011) Mg-chelatase H subunit affects ABA signaling in stomatal guard cells, but is not an ABA receptor in Arabidopsis thaliana. J Plant Res 124:527–538

    Article  PubMed  CAS  Google Scholar 

  • Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200

    Article  PubMed  CAS  Google Scholar 

  • Van Norman JM, Sieburth LE (2007) Dissecting the biosynthetic pathway for the bypass1 root-derived signal. Plant J 49:619–628

    Article  PubMed  CAS  Google Scholar 

  • Van Wijk KJ, Baginsky S (2011) Update on plastid proteomics in higher plants; current state and future goals. Plant Physiol 15:1578–1588

    Google Scholar 

  • Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S, Langebartels C, Seidlitz HK, Zabeau M, Van Montagu M, Inze D, Van Breusegem F (2004) Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J 39:45–58

    Article  PubMed  CAS  Google Scholar 

  • Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inze D, Van Breusegem F (2005) Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol 139:806–821

    Article  PubMed  CAS  Google Scholar 

  • von Gromoff ED, Alawady A, Meinecke L, Grimm B, Beck CF (2008) Heme, a plastid-derived regulator of nuclear gene expression in Chlamydomonas. Plant Cell 20:552–567

    Article  CAS  Google Scholar 

  • Wagner D, Przybyla D, Camp ROD, Kim C, Landgraf F, Lee KP, Wursch 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 

  • Walter MH, Floss DS, Strack D (2010) Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles. Planta 232:1–17

    Article  PubMed  CAS  Google Scholar 

  • Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447

    Article  PubMed  CAS  Google Scholar 

  • Weber AP, Linka N (2011) Connecting the plastid: transporters of the plastid envelope and their role in linking plastidial with cytosolic metabolism. Annu Rev Plant Biol 62:53–77

    Article  PubMed  CAS  Google Scholar 

  • Wilde A, Mikolajczyk S, Alawady A, Lokstein H, Grimm B (2004) The gun4 gene is essential for cyanobacterial porphyrin metabolism. FEBS Lett 571:119–123

    Article  PubMed  CAS  Google Scholar 

  • Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565

    Article  PubMed  CAS  Google Scholar 

  • Woitsch S, Römer S (2003) Expression of xanthophyll biosynthetic genes during light-dependent chloroplast differentiation. Plant Physiol 132:1508–1517

    Article  PubMed  CAS  Google Scholar 

  • Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9:383–395

    Article  PubMed  CAS  Google Scholar 

  • Woodson JD, Perez-Ruiz JM, Chory J (2011) Heme synthesis by plastid ferrochelatase I regulates nuclear gene expression in plants. Curr Biol 21:897–903

    Article  PubMed  CAS  Google Scholar 

  • Wu FQ, Xin Q, Cao Z, Liu ZQ, Du SY, Mei C, Zhao CX, Wang XF, Shang Y, Jiang T, Zhang XF, Yan L, Zhao R, Cui ZN, Liu R, Sun HL, Yang XL, Su Z, Zhang DP (2009) The magnesium-chelatase H subunit binds abscisic acid and functions in abscisic acid signaling: new evidence in Arabidopsis. Plant Physiol 150:1940–1954

    Article  PubMed  CAS  Google Scholar 

  • Yang DH, Andersson B, Aro EM, Ohad I (2001) The redox state of the plastoquinone pool controls the level of the light-harvesting chlorophyll a/b binding protein complex II (LHC II) during photoacclimation – cytochrome b(6)f deficient Lemna perpusilla plants are locked in a state of high-light acclimation. Photosynth Res 68:163–174

    Article  PubMed  CAS  Google Scholar 

  • Yoshida R, Sato T, Kanno A, Kameya T (1998) Streptomycin mimics the cool temperature response in rice plants. J Exp Bot 49:221–227

    CAS  Google Scholar 

  • Zeiger E, Talbott LD, Frechilla S, Srivastava A, Zhu J (2002) The guard cell chloroplast: a perspective for the twenty-first century. New Phytol 153:415–424

    CAS  Google Scholar 

  • Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song C-P (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448

    Google Scholar 

  • Zhang X, Tan L, Guo Z, Lu S, He S, Shu W, Zhou B (2009) Increased abscisic acid levels in transgenic tobacco over-expressing 9-cis-epoxycarotenoid dioxygenase influence H2O2 and NO production and antioxidant defences. Plant Cell Environ 32:509–519

    Article  PubMed  CAS  Google Scholar 

  • Zhou Y, Wang H, Gilmer S, Whitwill S, Fowke LC (2003) Effects of co-expressing the plant CDK inhibitor ICK1 and D-type cyclin genes on plant growth, cell size and ploidy in Arabidopsis thaliana. Planta 216:604–613

    PubMed  CAS  Google Scholar 

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Acknowledgments

Work in the laboratories of the authors has been supported by grants from the “Deutsche Forschungsgemeinschaft” to T.P. (PF 323-4, PF 323-5) and from the Spanish Government and Generalitat de Catalunya to S.M.B. (BFU2009-07294-E, BFU2009-06045, CSD2008-00040 and ICREA Academia prize).

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Pfannschmidt, T., Munné-Bosch, S. (2013). Plastid Signaling During the Plant Life Cycle. 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_22

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