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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
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
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
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
Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827
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
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
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
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
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
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
Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321
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
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
Beck CF (2001) Signaling pathways in chloroplast-to-nucleus communication. Protist 152:175–182
Beck CF (2005) Signaling pathways from the chloroplast to the nucleus. Planta 222:743–756
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
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
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
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
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
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
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
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
Buchanan BB, Gruissem W, Jones RL (2002) Biochemistry and molecular biology of plants. Wiley, Somerset
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
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
Cazzonelli CI (2011) Carotenoids in nature: insights from plants and beyond. Funct Plant Biol 38:833–847
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
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
Chamovitz D, Pecker I, Hirschberg J (1991) The molecular basis of resistance to the herbicide norflurazon. Plant Mol Biol 16:967–974
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
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
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
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
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
Demmig-Adams B, Adams WW III (2000) Photosynthesis – harvesting sunlight safely. Nature 403:373–374
Desikan R, Mackerness SAH, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172
Durnford DG, Falkowski PG (1997) Chloroplast redox regulation of nuclear gene transcription during photoacclimation. Photosynth Res 53:229–241
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
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
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
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
Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875
Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905
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
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
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
Giuliano G, Al-Babili S, von Lintig J (2003) Carotenoid oxygenases: cleave it or leave it. Trends Plant Sci 8:145–149
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
Gray JC, Sornarajah R, Zabron AA, Duckett CM, Khan MS (1995) Chloroplast control of nuclear gene expression. Photosynthesis, from light to biosphere. Kluwer, Dordrecht
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
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
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
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
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
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
Hörtensteiner S, Kräutler B (2011) Chlorophyll breakdown in higher plants. Biochim Biophys Acta 1807:977–988
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
Jarvis P (2007) Intracellular signalling: chloroplast backchat. Curr Biol 17:R552–R555
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
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
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
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
Kleine T, Voigt C, Leister D (2009) Plastid signalling to the nucleus: messengers still lost in the mists? Trends Genet 25:185–190
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
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
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
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
Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299:902–906
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
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136
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
López Ráez JA, Bouwmeester H (2008) Fine-tuning regulation of strigolactone biosynthesis under phosphate starvation. Plant Signal Behav 3:963–965
Lopez-Juez E, Pyke KA (2005) Plastids unleashed: their development and their integration in plant development. Int J Dev Biol 49:557–577
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
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
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
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
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
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
Mayfield SP, Nelson T, Taylor WC (1986) The fate of chloroplast proteins during photooxidation in carotenoid-deficient maize leaves. Plant Physiol 82:760–764
McCourt P, Creelman R (2008) The ABA receptor – we report you decide. Curr Opin Plant Biol 11:474–478
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
Métraux JP (2002) Recent breakthroughs in the study of salicylic acid biosynthesis. Trends Plant Sci 7:332–334
Milanowska J, Gruczecki W (2005) Heat-induced and light-induced isomerization of the xanthophyll pigment zeaxanthin. J Photochem Photobiol B Biol 80:178–186
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498
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
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
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
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
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
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
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
Mullineaux PM, Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5:43–48
Mullineaux PM, Rausch T (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynth Res 86:459–474
Munné-Bosch S (2008) Do perennials really senesce? Trends Plant Sci 13:216–220
Munné-Bosch S, Alegre L (2002) The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21:31–57
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
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
Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185
Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460
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
Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57:739–759
Oelmüller R (1989) Photooxidative destruction of chloroplasts and its effect on nuclear gene-expression and extraplastidic enzyme levels. Photochem Photobiol 49:229–239
Oelmüller R, Mohr H (1986) Photooxidative destruction of chloroplasts and its consequences for expression of nuclear genes. Planta 167:106–113
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
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
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
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
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
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
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
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
Pesaresi P, Schneider A, Kleine T, Leister D (2007) Interorganellar communication. Curr Opin Plant Biol 10:600–606
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
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
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
Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8:33–41
Pfannschmidt T (2010) Plastidial retrograde signalling – a true “plastid factor” or just metabolite signatures? Trends Plant Sci 15:427–435
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
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
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
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
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
Pogson BJ, Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development: an overview. Plant Physiol 155:1545–1551
Pogson BJ, Woo NS, Förster B, Small ID (2008) Plastid signalling to the nucleus and beyond. Trends Plant Sci 13:602–609
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
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
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
Rodermel S (2001) Pathways of plastid-to-nucleus signaling. Trends Plant Sci 6:471–478
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
Schaller F (2001) Enzymes of the biosynthesis of octadecanoid-derived signaling molecules. J Exp Bot 52:11–23
Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874
Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7:41–48
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
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
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
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
Smart CM (1994) Gene expression during leaf senescence. New Phytol 126:418–449
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
Stoebe B, Maier UG (2002) One, two, three: nature’s tool box for building plastids. Protoplasma 219:123–130
Strand A (2004) Plastid-to-nucleus signalling. Curr Opin Plant Biol 7:621–625
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
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
Sugiura M (1992) The chloroplast genome. Plant Mol Biol 19:149–168
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
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
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
Surpin M, Larkin RM, Chory J (2002) Signal transduction between the chloroplast and the nucleus. Plant Cell 14:S327–S338
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
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
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
Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346
Taylor WC (1989) Regulatory interactions between nuclear and plastid genomes. Annu Rev Plant Physiol 40:211–233
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
Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135
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
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
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
Van Norman JM, Sieburth LE (2007) Dissecting the biosynthetic pathway for the bypass1 root-derived signal. Plant J 49:619–628
Van Wijk KJ, Baginsky S (2011) Update on plastid proteomics in higher plants; current state and future goals. Plant Physiol 15:1578–1588
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
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
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
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
Walter MH, Floss DS, Strack D (2010) Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles. Planta 232:1–17
Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447
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
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
Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565
Woitsch S, Römer S (2003) Expression of xanthophyll biosynthetic genes during light-dependent chloroplast differentiation. Plant Physiol 132:1508–1517
Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9:383–395
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
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
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
Yoshida R, Sato T, Kanno A, Kameya T (1998) Streptomycin mimics the cool temperature response in rice plants. J Exp Bot 49:221–227
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
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
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
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
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).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
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
Download citation
DOI: https://doi.org/10.1007/978-94-007-5724-0_22
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-5723-3
Online ISBN: 978-94-007-5724-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)