Abstract
DNA and the machinery for gene expression have been discovered in chloroplasts during the 1960s. It was soon evident that the chloroplast genome is small, that many genes for chloroplast-localized proteins must reside in the nucleus, and that the expression of the genes in both cellular compartments must be coordinated. In the 1970s, the first evidence for plastid signals controlling nuclear gene expression was provided for plastid ribosome-deficient mutants. This review describes the discovery and the first studies on plastid-to-nucleus signaling. Today, many retrograde signals are known, which coordinate plastid and nuclear gene expression during the development of the organelle and in response to environmental changes. The nucleus receives information about the flux through the heme branch of the tetrapyrrole pathway, the expression of plastid genes, the metabolite stage in the organelle, and the efficiency of the photosynthetic electron flow. Singlet oxygen generated during light stress and breakdown products of carotenoids initiate signaling events in the organelle which alter nuclear gene expression. Operational signals permanently coordinate gene expression in both organelles. The biosynthesis of phytohormones like jasmonic, salicylic, and abscisic acids or cytokinins starts in the plastids, and these hormones became crucial players in coordinating plastid and nuclear gene expression under stress. Methylerythritol cyclodiphosphate, a biochemical intermediate of the methylerythritol phosphate pathway, alters the chromatin structure in the nucleus which in turn affects the expression of a particular subset of stress-inducible genes. Dual targeted proteins with plastid and nuclear locations participate in the interorganellar communication. We discuss our current knowledge about retrograde signaling and address open questions.
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Abbreviations
- ABI4:
-
abscisic acid insensitive 4
- β-CC:
-
β-cyclocitral
- GLK1/2:
-
golden 2-like 1/2
- GUN1/4/5:
-
genomes uncoupled 1/4/5
- EX1/EX2:
-
executer 1/2
- HDS1:
-
hydroxymethylbutenyl diphosphate synthase
- LHCB:
-
gene-encoding photosystem II chlorophyll a/b binding protein
- MEcPP:
-
methylerythritol cyclodiphosphate
- Mg-protop-IX:
-
Mg-protoporphyrin IX
- ΔPET:
-
impairment of photosynthetic electron transport chain
- PGE:
-
plastid gene expression
- PhANG:
-
photosynthesis-Associated Nuclear Genes
- PQ:
-
plastoquinone
- PRIN2:
-
plastid redox-insensitive 2
- PSI:
-
photosystem I
- ROS:
-
reactive oxygen species
- SAL1:
-
inositol polyphosphate 1-phosphatase
- TFs:
-
transcription factors
- STN7:
-
thylakoid protein kinase 7
- WHY1:
-
whirly 1
References
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
Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321
Avendaño-Vázquez AO, Cordoba E, Llamas E, San Román C, Nisar N, De la Torre S, Ramos-Vega M, de la Luz Gutiérrez-Nava M, Cazzonelli CI, Pogson BJ, León P (2014) An uncharacterized apocarotenoid-derived signal generated in ζ-carotene desaturase mutants regulates leaf development and the expression of chloroplast and nuclear genes in Arabidopsis. Plant Cell 26:2524–2537
Baier M, Stroher E, Dietz KJ (2004) The acceptor availability at photosystem I and ABA control nuclear expression of 2-Cys peroxiredoxin-A in Arabidopsis thaliana. Plant Cell Physiol 45:997–1006
Bajracharya D, Bergfield R, Hatzfeld W-D, Klein S, Schopfer P (1987) Regulatory involvement of plastids in the development of peroxisomal enzymes in the cotyledons of mustard (Sinapis alba L.) seedlings. J Plant Physiol 126:421–436
Banerjee A, Sharkey TD (2014) Methylerythritol 4-phosphate (MEP) pathway metabolic regulation. Nat Prod Rep 31:1043–1055
Barajas-López J de D, Blanco NE, Strand Å (2013) Plastid-to-nucleus communication, signals controlling the running of the plant cell. Biochim Biophys Acta 1833:425–437
Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442
Batschauer A, Mösinger E, Kreuz K, Dörr I, Apel K (1986) The implications of a plastid-derived factor in the transcriptional control of nuclear genes encoding the light-harvesting chlorophyll a/b protein. Eur J Biochem 154:625–634
Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895
Berglund AK, Spånning E, Biverståhl H, Maddalo G, Tellgren-Roth C, Mäler L, Glaser E (2009) Dual targeting to mitochondria and chloroplasts: characterization of Thr-tRNA synthetase targeting peptide. Mol Plant 2:1298–1309
Bernardi G (1979) The petite mutation in yeast. Trends Biochem Sci 4:197–201
Blair GE, Ellis RJ (1973) Protein synthesis in chloroplasts. I. Light-driven synthesis of the large subunit of fraction I protein by isolated pea chloroplasts. Biochim Biophys Acta 319:223–234
Bogorad L (1975) Evolution of organelles and eukaryotic genomes. Science 188:891–898
Bolle C, Sopory S, Lübberstedt T, Klösgen RB, Herrmann RG, Oelmüller R (1994) The role of plastids in the expression of nuclear genes for thylakoid proteins studied with chimeric β-glucuronidase gene fusions. Plant Physiol 105:1355–1364
Bolle C, Kusnetsov VV, Herrmann RG, Oelmüller R (1996a) The spinach AtpC and AtpD genes contain elements for light-regulated, plastid-dependent and organ-specific expression in the vicinity of the transcription start sites. Plant J 9:21–30
Bolle C, Herrmann RG, Oelmüller R (1996b) Intron sequences are involved in the plastid- and light-dependent expression of the spinach PsaD gene. Plant J 10:919–924
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
Börner T (2017) The discovery of plastid-to-nucleus retrograde signaling-a personal perspective. Protoplasma 254:1845–1855
Börner T, Knoth R, Herrmann F, Hagemann R (1972) Struktur und Funktion der genetischen Information in den Plastiden. V. Das Fehlen von ribosomaler RNS in den Plastiden der Plastommutante “Mrs. Parker” von Pelargonium zonale Ait. Theor Appl Genet 42:3–11
Börner T, Herrmann FH, Hagemann R (1973) Plastid ribosome deficient mutants in Pelargonium zonale. FEBS Lett 37:17–19
Börner T, Knoth R, Herrmann F, Hagemann R (1974) Struktur und Funktion der genetischen Information in den Plastiden. X. Das Fehlen von Fraktion-I-Protein in den weißen Plastiden einiger Sorten von Pelargonium zonale. Biochem Physiol Pflanz 165:429–432
Börner T, Schumann B, Hagemann R (1976) Biochemical studies on a plastid ribosome-deficient mutant of Hordeum vulgare. In: Bücher T, Neupert W, Sebald W, Werner S (eds) Genetics and biogenesis of chloroplasts and mitochondria. Elsevier/North-Holland Medical Press, Amsterdam, pp 41–48
Börner T, Mendel RR, Schiemann J (1986) Nitrate reductase is not accumulated in chloroplast-ribosome-deficient mutants of higher plants. Planta 169:202–207
Bradbeer JW, Börner T (1978) Activities of glyceraldehyde-dephosphate dehydrogenase (NADP+) and phosphoribulokinase in two barley mutants deficient in chloroplast ribosomes. In: Akoyunoglou G, Argyroudi-Akoyunoglou JG (eds) Chloroplast development. North Holland, Amsterdam, pp 727–732
Bradbeer JW, Atkinson YE, Börner T, Hagemann R (1979) Cytoplasmic synthesis of plastid polypeptides may be controlled by plastid-synthesised RNA. Nature 279:816–817
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
Brunkard JO, Burch-Smith TM (2018) Ties that bind: the integration of plastid signalling pathways in plant cell metabolism. Essays Biochem 62:95–107
Burch-Smith TM, Brunkard JO, Choi YG, Zambryski PC (2011) Organelle-nucleus cross-talk regulates plant intercellular communication via plasmodesmata. Proc Natl Acad Sci U S A 108:E1451–E1460
Burgess DG, Taylor WC (1988) Chloroplast photooxidation affects the transcription of a nuclear gene family. Mol Gen Genet 214:89–96
Butow RA, Avadhani NG (2004) Mitochondrial signaling: the retrograde response. Mol Cell 14:1–15
Cappadocia L, Maréchal A, Parent JS, Lepage E, Sygusch J, Brisson N (2010) Crystal structures of DNA-Whirly complexes and their role in Arabidopsis organelle genome repair. Plant Cell 22:1849–1867
Cappadocia L, Parent JS, Zampini E, Lepage E, Sygusch J, Brisson N (2012) A conserved lysine residue of plant Whirly proteins is necessary for higher order protein assembly and protection against DNA damage. Nucleic Acids Res 40:258–269
Chan PH, Wildman SG (1972) Chloroplast DNA codes for the primary structure of the large subunit of fraction I protein. Biochim Biophys Acta 277:677–680
Chan KX, Crisp PA, Estavillo GM, Pogson BJ (2010) Chloroplast-to-nucleus communication: current knowledge, experimental strategies and relationship to drought stress signaling. Plant Signal Behav 5:1575–1582
Chan KX, Phua SY, Crisp P, McQuinn R, Pogson BJ (2016) Learning the languages of the chloroplast: retrograde signaling and beyond. Annu Rev Plant Biol 67:25–53
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
Chi W, Sun X, Zhang L (2013) Intracellular signaling from plastid to nucleus. Annu Rev Plant Biol 64:559–582
Chi W, Feng P, Ma J, Zhang L (2015) Metabolites and chloroplast retrograde signaling. Curr Opin Plant Biol 25:32–38
Colombo M, Tadini L, Peracchio C, Ferrari R, Pesaresi P (2016) GUN1, a Jack-of-all-trades in chloroplast protein homeostasis and signaling. Front Plant Sci 7:1427
Criddle RS, Dau B, Kleinkopf DE, Huffaker RC (1970) Differential synthesis of ribulose diphosphate subunits. Biochem Biophys Res Commun 41:621–627
de Souza A, Wang JZ, Dehesh K (2017) Retrograde signals: integrators of interorganellar communication and orchestrators of plant development. Annu Rev Plant Biol 68:85–108
Demmig-Adams B, Stewart JJ, Adams WW 3rd (2017) Environmental regulation of intrinsic photosynthetic capacity: an integrated view. Curr Opin Plant Biol 37:34–41
Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF (2011) Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9:e0156
Desveaux D, Després C, Joyeux A, Subramaniam R, Brisson N (2000) PBF-2 is a novel single-stranded DNA binding factor implicated in PR-10a gene activation in potato. Plant Cell 12:1477–1489
Desveaux D, Subramaniam R, Després C, Mess JN, Lévesque C, Fobert PR, Dangl JL, Brisson N (2004) A “Whirly” transcription factor is required for salicylic acid-dependent disease resistance in Arabidopsis. Dev Cell 6:229–240
Dietz KJ (2016) Thiol-Based peroxidases and ascorbate peroxidases: why plants rely on multiple peroxidase systems in the photosynthesizing chloroplast? Mol Cells 39:20–25
Dietz KJ, Vogel MO, Viehhauser A (2010) AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signalling. Protoplasma 245:3–14
Dietz KJ, Turkan I, Krieger-Liszkay A (2016) Redox- and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast. Plant Physiol 171:1541–1550
Dietzel L, Bräutigam K, Pfannschmidt T (2008) Photosynthetic acclimation: state transitions and adjustment of photosystem stoichiometry – functional relationships between short-term and long-term light quality acclimation in plants. FEBS J 275:1080–1088
Dietzel L, Gläßer C, Liebers M, Hiekel S, Courtois F, Czarnecki O, Schlicke H, Zubo Y, Börner T, Mayer K, Grimm B, Pfannschmidt T (2015) Identification of early nuclear target genes of plastidial redox signals that trigger the long-term response of Arabidopsis to light quality shifts. Mol Plant 8:1237–1252
Dogra V, Duan J, Lee KP, Lv S, Liu R, Kim C (2017) FtsH2-dependent proteolysis of EXECUTER1 Is essential in mediating singlet oxygen-triggered retrograde signaling in Arabidopsis thaliana. Front Plant Sci 8:1145
Dörmann P, Kim H, Ott T, Schulze-Lefert P, Trujillo M, Wewer V, Hückelhoven R (2014) Cell-autonomous defense, re-organization and trafficking of membranes in plant-microbe interactions. New Phytol 204:815–822
Duanmu D, Casero D, Dent RM, Gallaher S, Yang W, Rockwell NC, Martin SS, Pellegrini M, Niyogi KK, Merchant SS, Grossman AR, Lagarias JC (2013) Retrograde bilin signaling enables Chlamydomonas greening and phototrophic survival. Proc Natl Acad Sci U S A 110:3621–3626
Eguchi S, Takano H, Ono K, Takio S (2002) Photosynthetic electron transport regulates the stability of the transcript for the protochlorophyllide oxidoreductase gene in the liverwort, Marchantia paleacea var. diptera. Plant Cell Physiol 43:573–577
Eisenhut M, Hocken N, Weber AP (2015) Plastidial metabolite transporters integrate photorespiration with carbon, nitrogen, and sulfur metabolism. Cell Calcium 58:98–104
Ellis RJ (1975) Inhibition of plastid protein synthesis by lincomycin and 2-(4-methyl-2,6-dinitroanilino)-N-methylpropionamide. Phytochemistry 14:89–93
Ellis RJ (1977) Protein synthesis by isolated chloroplasts. Biochim Biophys Acta 463:285–315
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 U S A 92:10237–11041
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
Estavillo GM, Chan KX, Phua SY, Pogson BJ (2013) Reconsidering the nature and mode of action of metabolite retrograde signals from the chloroplast. Front Plant Sci 3:300
Farmer EE, Mueller MJ (2013) ROS-mediated lipid peroxidation and RES-activated signaling. Annu Rev Plant Biol 64:429–450
Feierabend J (1977) Capacity for chlorophyll synthesis in heat-bleached 70S ribosome-deficient rye leaves. Planta 135:83–88
Feierabend J, Mikus M (1977) Occurrence of a high temperature sensitivity of chloroplast ribosome formation in several higher plants. Plant Physiol 59:863–867
Feierabend J, Schrader-Reichhardt U (1976) Biochemical differentiation of plastids and other organelles in rye leaves with a high-temperature-induced deficiency of plastid ribosomes. Planta 129:133–145
Fernández AP, Strand A (2008) Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Curr Opin Plant Biol 11:509–513
Fey V, Wagner R, Braütigam 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
Flügge UI, Häusler RE, Ludewig F, Gierth M (2011) The role of transporters in supplying energy to plant plastids. J Exp Bot 62:2381–2392
Foyer CH, Karpinska B, Krupinska K (2014) The functions of WHIRLY1 and REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis. Philos Trans R Soc Lond Ser B Biol Sci 369:20130226
Galvez-Valdivieso G, Mullineaux PM (2010) The role of reactive oxygen species in signalling from chloroplasts to the nucleus. Physiol Plant 138:430–439
Garcion C, Lohmann A, Lamodière E, Catinot J, Buchala A, Doermann P, Métraux JP (2008) Characterization and biological function of the ISOCHORISMATE SYNTHASE2 gene of Arabidopsis. Plant Physiol 147:1279–1287
Ge C, Spånning E, Glaser E, Wieslander A (2014) Import determinants of organelle-specific and dual targeting peptides of mitochondria and chloroplasts in Arabidopsis thaliana. Mol Plant 7:121–136
Gigolashvili T, Geier M, Ashykhmina N, Frerigmann H, Wulfert S, Krueger S, Mugford SG, Kopriva S, Haferkamp I, Flügge UI (2012) Much more than a thylakoid ADP/ATP carrier– enlightening a role of TAAC in plastidic phosphoadenosine 50-phosphosulfate (PAPS) supply to the cytosol. Plant Cell 24:4187–4204
Gile GH, Moog D, Slamovits CH, Maier UG, Archibald JM (2015) Dual organellar targeting of aminoacyl-tRNA synthetases in diatoms and cryptophytes. Genome Biol Evol 7:1728–1742
Giuliano G, Scolnik PA (1988) Transcription of two photosynthesis-associated nuclear gene families correlates with the presence of chloroplasts in leaves of the variegated tomato ghost mutant. Plant Physiol 86:7–9
Givan AL, Criddle RS (1972) Ribulose diphosphate carboxylase from Chlamydomonas reinhardi: purification, properties and mode of synthesis in the cell. Arch Biochem Biophys 149:153–154
Godoy Herz MA, Kornblihtt AR, Barta A, Kalyna M, Petrillo E (2014) Shedding light on the chloroplast as a remote control of nuclear gene expression. Plant Signal Behav 9:e976150
Gollan PJ, Tikkanen M, Aro EM (2015) Photosynthetic light reactions: integral to chloroplast retrograde signalling. Curr Opin Plant Biol 27:180–191
Grabowski E, Miao Y, Mulisch M, Krupinska K (2008) Single-stranded DNA-binding protein Whirly1 in barley leaves is located in plastids and the nucleus of the same cell. Plant Physiol 147:1800–1804
Gray JC, Sornarajah R, Zabron AA, Duckett CM, Khan MS (1995) Chloroplast control of nuclear gene expression. In: Mathis P (ed) Photosynthesis, from light to biosphere. Kluwer, Dordrecht, pp 543–550
Greiner S, Bock R (2013) Tuning a menage a trois: co-evolution and co-adaptation of nuclear and organellar genomes in plants. BioEssays 35:354–365
Grieshaber NA, Fischer ER, Mead DJ, Dooley CA, Hackstadt T (2004) Chlamydial histone-DNA interactions are disrupted by a metabolite in the methylerythritol phosphate pathway of isoprenoid biosynthesis. Proc Natl Acad Sci U S A 101:7451–7756
Grieshaber NA, Sager JB, Dooley CA, Hayes SF, Hackstadt T (2006) Regulation of the Chlamydia trachomatis histone H1-like protein Hc2 is IspE dependent and IhtA independent. J Bacteriol 188:5289–5292
Guo H, Feng P, Chi W, Sun X, Xu X, Li Y, Ren D, Lu C, Rochaix JD, Leister D, Zhang L (2016) Plastid-nucleus communication involves calcium-modulated MAPK signalling. Nat Commun 7:12173
Hagemann R, Börner T (1987) Plastid ribosome-deficient mutants of higher plants as a tool in studying chloroplast biogenesis. In: Akoyunoglou G, Argyroudi-Akoyunoglou JG (eds) Chloroplast development. North Holland, Amsterdam, pp 709–720
Han GZ (2017) Evolution of jasmonate biosynthesis and signaling mechanisms. J Exp Bot 68:1323–1331
Hanke G, Mulo P (2013) Plant type ferredoxins and ferredoxin-dependent metabolism. Plant Cell Environ 36:1071–1084
Harpster MH, Mayfield SP, Taylor WC (1984) Effects of pigment-deficient mutants on the accumulation of photosynthetic proteins in maize. Plant Mol Biol 3:258–263
Hawkesford MJ, De Kok LJ (2006) Managing sulphur metabolism in plants. Plant Cell Environ 29:382–395
Hernández-Verdeja T, Strand Å (2018) Retrograde signals navigate the path to chloroplast development. Plant Physiol 176:967–976
Hess WR, Müller A, Nagy F, Börner T (1994) Ribosome-deficient plastids affect transcription of light-induced nuclear genes: genetic evidence for a plastid-derived signal. Mol Gen Genet 242:305–312
Huang J, Gu M, Lai Z, Fan B, Shi K, Zhou YH, Yu JQ, Chen Z (2010) Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol 153:1526–1538
Huang H, Liu B, Liu L, Song S (2017) Jasmonate action in plant growth and development. J Exp Bot 68:1349–1359
Inaba T (2010) Bilateral communication between plastid and the nucleus: plastid protein import and plastid-to-nucleus retrograde signaling. Biosci Biotechnol Biochem 74:471–476
Inaba T, Yazu F, Ito-Inaba Y, Kakizaki T, Nakayama K (2011) Retrograde signaling pathway from plastid to nucleus. Int Rev Cell Mol Biol 290:167–204
Isemer R, Mulisch M, Schafer A, Kirchner S, Koop HU, Krupinska K (2012) Recombinant Whirly1 translocates from transplastomic chloroplasts to the nucleus. FEBS Lett 586:85–88
Johanningmeier U, Howell SH (1984) Regulation of light-harvesting chlorophyll-binding protein messenger-RNA accumulation in Chlamydomonas rheinhardi – possible involvement of chlorophyll synthesis precursors. J Biol Chem 259:3541–3549
Jung HS, Crisp PA, Estavillo GM, Cole B, Hong F, Mockler TC, Pogson BJ, Chory J (2013) Subset of heat-shock transcription factors required for the early response of Arabidopsis to excess light. Proc Natl Acad Sci U S A 110:1447–1479
Karlsson PM, Herdean A, Adolfsson L, Beebo A, Nziengui H, Irigoyen S, Ünnep R, Zsiros O, Nagy G, Garab G, Aronsson H, Versaw WK, Spetea C (2015) The Arabidopsis thylakoid transporter PHT4;1 influences phosphate availability for ATP synthesis and plant growth. Plant J 84:99–110
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
Karpiński S, Szechyńska-Hebda M, Wituszyńska W, Burdiak P (2013) Light acclimation, retrograde signalling, cell death and immune defences in plants. Plant Cell Environ 36:736–744
Kim C, Apel K (2013a) Singlet oxygen-mediated signaling in plants: moving from flu to wild type reveals an increasing complexity. Photosynth Res 116:455–464
Kim C, Apel K (2013b) O2-mediated and EXECUTER-dependent retrograde plastid-to-nucleus signaling in norflurazon-treated seedlings of Arabidopsis thaliana. Mol Plant 6:1580–1591
Kindgren P, Kremnev D, Blanco NE, de Dios Barajas López J, Fernández AP, Tellgren-Roth C, Kleine T, Small I, Strand A (2012) The plastid redox insensitive 2 mutant of Arabidopsis is impaired in PEP activity and high light-dependent plastid redox signalling to the nucleus. Plant J 70:279–291
Kirk JTO (1971) Chloroplast structure and biogenesis. Annu Rev Biochem 40:161–196
Kirk JTO, Tilney-Bassett RAE (1967) The plastids. Freeman, London
Klein M, Papenbrock J (2004) The multi-protein family of Arabidopsis sulphotransferases and their relatives in other plant species. J Exp Bot 55:1809–1820
Kleine T, Leister D (2016) Retrograde signaling: organelles go networking. Biochim Biophys Acta 1857:1313–1325
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
Krause K, Krupinska K (2009) Nuclear regulators with a second home in organelles. Trends Plant Sci 14:194–199
Krause K, Kilbienski I, Mulisch M, Rödiger A, Schäfer A, Krupinska K (2005) DNA-binding proteins of the Whirly family in Arabidopsis thaliana are targeted to the organelles. FEBS Lett 579:3707–3712
Krause K, Oetke S, Krupinska K (2012) Dual targeting and retrograde translocation: regulators of plant nuclear gene expression can be sequestered by plastids. Int J Mol Sci 13:11085–11101
Kropat J, Oster U, Rüdiger W, Beck CF (1997) Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proc Natl Acad Sci U S A 94:14168–14172
Kropat J, Oster U, Rüdiger W, Beck CF (2000) Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. Plant J 24:523–531
Krupinska K, Dähnhardt D, Fischer-Kilbienski I, Kucharewicz W, Scharrenberg C, Trösch M, Buck F (2013) Identification of WHIRLY1 as a factor binding to the promoter of the stress and senescence-associated gene HvS40. J Plant Growth Regul 33:91
Kusnetsov V, Bolle C, Lübberstedt T, Sopory S, Herrmann RG, Oelmüller R (1996) Evidence that the plastid signal and light operate via the same cis-acting elements in the promoters of nuclear genes for plastid proteins. Mol Gen Genet 252:631–639
Kusnetsov V, Landsberger M, Meurer J, Oelmüller R (1999) The assembly of the CAAT-box binding complex at a photosynthesis gene promoter is regulated by light, cytokinin, and the stage of the plastids. J Biol Chem 274:36009–36014
Laloi C, Przybyla D, Apel K (2006) A genetic approach towards elucidating the biological activity of different reactive oxygen species in Arabidopsis thaliana. J Exp Bot 57:1719–1724
Langner U, Baudisch B, Klösgen RB (2014) Organelle import of proteins with dual targeting properties into mitochondria and chloroplasts takes place by the general import pathways. Plant Signal Behav 9:e29301
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 U S A 104:10270–10275
Leister D (2005) Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis. Gene 354:110–116
Leister D (2016) Towards understanding the evolution and functional diversification of DNA-containing plant organelles. F1000 Res 5:330
Lemos M, Xiao Y, Bjornson M, Wang JZ, Hicks D, Ad S, Wang CQ, Yang P, Ma S, Dinesh-Kumar S, Dehesh K (2016) The plastidial retrograde signal methyl erythritol cyclopyrophosphate is a regulator of salicylic acid and jasmonic acid crosstalk. J Exp Bot 67:1557–1566
Lepage É, Zampini É, Brisson N (2013) Plastid genome instability leads to reactive oxygen species production and plastid-to-nucleus retrograde signaling in Arabidopsis. Plant Physiol 163:867–881
Lepistö A, Rintamäki E (2012) Coordination of plastid and light signaling pathways upon development of Arabidopsis leaves under various photoperiods. Mol Plant 5:799–816
Lepistö A, Toivola J, Nikkanen L, Rintamäki E (2012) Retrograde signaling from functionally heterogeneous plastids. Front Plant Sci 3:286
Li B, Kronzucker HJ, Shi W (2013) Molecular components of stress-responsive plastid retrograde signaling networks and their involvement in ammonium stress. Plant Signal Behav 8:e23107
Linka N, Theodoulou FL (2013) Metabolite transporters of the plant peroxisomal membrane: known and unknown. Subcell Biochem 69:169–194
Linka N, Weber AP (2010) Intracellular metabolite transporters in plants. Mol Plant 3:21–53
Lübberstedt T, Oelmüller R, Wanner G, Herrmann RG (1994) The role of plastids in the expression of nuclear genes for thylakoid proteins studied with chimeric β-glucuronidase gene fusions. Plant Physiol 105:1355–1364
Lurin C, Andrés C, Aubourg S, Bellaoui M, Bitton F, Bruyère C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniette ML, Mireau H, Peeters N, Renou JP, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089–2103
Lv F, Zhou J, Zeng L, Xing D (2015) β-Cyclocitral upregulates salicylic acid signalling to enhance excess light acclimation in Arabidopsis. J Exp Bot 66:4719–4732
Macaulay KM, Heath GA, Ciulli A, Murphy AM, Abell C, Carr JP, Smith AG (2017) The biochemical properties of the two Arabidopsis thaliana isochorismate synthases. Biochem J 474:1579–1590
Mach J (2018) The lipase Link: abscisic acid induces PLASTID LIPASES, which produce Jasmonic acid precursors. Plant Cell 30(5):948–949
Martin G, Leivar P, Ludevid D, Tepperman JM, Quail PH, Monte E (2016) Phytochrome and retrograde signalling pathways converge to antagonistically regulate a light-induced transcriptional network. Nat Commun 7:11431
Martínez C, Pons E, Prats G, León J (2004) Salicylic acid regulates flowering time and links defence responses and reproductive development. Plant J 37:209–217
Maruta T, Noshi M, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2012) H2O2-triggered retrograde signaling from chloroplasts to nucleus plays specific role in response to stress. J Biol Chem 287:11717–11729
Maruta T, Sawa Y, Shigeoka S, Ishikawa T (2016) Diversity and evolution of ascorbate peroxidase functions in chloroplasts: more than just a classical antioxidant enzyme? Plant Cell Physiol 57:1377–1386
Maxwell DP, Laudenbach DE, Huner N (1995) Redox regulation of light-harvesting complex II and cab mRNA 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 (LHCP) mRNA. Eur J Biochem 144:79–84
Mayfield SP, Taylor WV (1987) Chloroplast photooxidation inhibits the expression of a set of nuclear genes. Mol Gen Genet 208:309–314
Mazzoleni M, Figuet S, Martin-Laffon J, Mininno M, Gilgen A, Leroux M, Brugière S, Tardif M, Alban C, Ravanel S (2015) Dual targeting of the protein methyltransferase PrmA contributes to both chloroplastic and mitochondrial ribosomal protein L11 methylation in Arabidopsis. Plant Cell Physiol 56:1697–1710
Mehrshahi P, Johnny C, DellaPenna D (2014) Redefining the metabolic continuity of chloroplasts and ER. Trends Plant Sci 19:501–507
Melonek J, Mulisch M, Schmitz-Linneweber C, Grabowski E, Hensel G, Krupinska K (2010) Whirly1 in chloroplasts associates with intron containing RNAs and rarely co-localizes with nucleoids. Planta 232:471–481
Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp R, Apel K (2001) FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A 98:12826–12831
Miao Y, Jiang J, Ren Y, Zhao Z (2013) The single-stranded DNA-binding protein WHIRLY1 represses WRKY53 expression and delays leaf senescence in a developmental stage-dependent manner in Arabidopsis. Plant Physiol 163:746–756
Millar AH, Whelan J, Small I (2006) Recent surprises in protein targeting to mitochondria and plastids. Curr Opin Plant Biol 9:610–615
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 U S A 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 U S A 105:15184–15189
Mohr H, Neininger A, Seith B (1992) Control of nitrate reductase and nitrite reductase gene expression by light, nitrate and a plastidic factor. Bot Acta 105:81–89
Morris K, MacKerness SA, 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
Moulin M, McCormac AC, Terry MJ, Smith AG (2008) Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc Natl Acad Sci U S A 105:15178–15183
Nevarez PA, Qiu Y, Inoue H, Yoo CY, Benfey PN, Schnell DJ, Chen M (2017) Mechanism of dual targeting of the phytochrome signaling component HEMERA/pTAC12 to plastids and the nucleus. Plant Physiol 173:1953–1966
Nomura H, Komori T, Uemura S, Kanda Y, Shimotani K, Nakai K, Furuichi T, Takebayashi K, Sugimoto T, Sano S, Suwastika IN, Fukusaki E, Yoshioka H, Nakahira Y, Shiina T (2012) Chloroplast-mediated activation of plant immune signalling in Arabidopsis. Nat Commun 3:926
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 l49:229–239
Oelmüller R, Briggs WR (1990) Intact plastids are required for nitrate- and light-induced accumulation of nitrate reductase activity and mRNA in squash cotyledons. Plant Physiol 92:434–439
Oelmüller R, Mohr H (1986) Photooxidative destruction of chloroplasts and its consequences for expression of nuclear genes. Planta 167:106–113
Oelmüller R, Schuster C (1987) Inhibition and promotion by light of the accumulation of translatable mRNA of the light-harvesting chlorophyll a/b-binding protein of photosystem II. Planta 172:60–70
Oelmüller R, Dietrich G, Link G, Mohr H (1986a) Regulatory factors involved in gene expression (subunits of ribulose-1,5-bisphosphate carboxylase) in mustard (Sinapis alba L.) cotyledons. Planta 169:260–266
Oelmüller R, Levitan I, Bergfeld R, Rajasekhar VK, Mohr H (1986b) Expression of nuclear genes as affected by treatments acting on the plastids. Planta 168:482–492
Oelmüller R, Schuster C, Mohr H (1988) Physiological characterization of a plastidic signal required for nitrate-induced appearance of nitrate and nitrite reductases. Planta 174:75–83
Oelmüller R, Bolle C, Tyagi AK, Niekrawietz N, Breit S, Herrmann RG (1993) Characterization of the promoter from the single-copy gene encoding ferredoxin-NADP+-oxidoreductase from spinach. Mol Gen Genet 237:261–272
op den Camp R, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Göbel 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
Ostrovsky D, Kharatian E, Malarova I, Shipanova I, Sibeldina L, Shashkov A, Tantsirev G (1992) Synthesis of a new organic pyrophosphate in large quantities is induced in some bacteria by oxidative stress. Biofactors 3:261–264
Ostrovsky D, Diomina G, Lysak E, Matveeva E, Ogrel O, Trutko S (1998) Effect of oxidative stress on the biosynthesis of 2-C-methyl-d-erythritol-2,4-cyclopyrophosphate and isoprenoids by several bacterial strains. Arch Microbiol 171:69–72
Otori K, Tanabe N, Maruyama T, Sato S, Yanagisawa S, Tamoi M, Shigeoka S (2017) Enhanced photosynthetic capacity increases nitrogen metabolism through the coordinated regulation of carbon and nitrogen assimilation in Arabidopsis thaliana. J Plant Res 130:909–927
Padmanabhan MS, Dinesh-Kumar SP (2010) All hands on deck—the role of chloroplasts, endoplasmic reticulum and the nucleus in driving plant innate immunity. Mol Plant-Microbe Interact 23:1368–1380
Page MT, Kacprzak SM, Mochizuki N, Okamoto H, Smith AG, Terry MJ (2017) Seedlings lacking the PTM protein do not show a genomes uncoupled (gun) mutant phenotype. Plant Physiol 174:21–26
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 P, Leister D (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21:2402–2423
Pesaresi P, Pribil M, Wunder T, Leister D (2011) Dynamics of reversible protein phosphorylation in thylakoids of flowering plants: the roles of STN7, STN8 and TAP38. Biochim Biophys Acta 1807:887–896
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 U S A 95:9009–9013
Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmüller R (2006) pTAC2, -6 and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18:176–197
Pfalz J, Liebers M, Hirth M, Grübler B, Holtzegel U, Schröter Y, Dietzel L, Pfannschmidt T (2012) Environmental control of plant nuclear gene expression by chloroplast redox signals. Front Plant Sci 3:257
Pfannschmidt T, Nilsson A, Tullberg A, Link G, Allen JF (1999) Direct transcriptional control of the chloroplast genes psbA and psaAB adjusts photosynthesis to light energy distribution in plants. IUBMB Life 48:271–276
Pfannschmidt T, Schütze 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, Schütze 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
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, Woo NS, Förster B, Small ID (2008) Plastid signalling to the nucleus and beyond. Trends Plant Sci 13:602–609
Poulsen C, Verpoorte R (1991) Roles of chorismate mutase, isochorismate synthase and anthranilate synthase in plants. Phytochemistry 30:377–386
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
Przybyla-Toscano J, Roland M, Gaymard F, Couturier J, Rouhier N (2018) Roles and maturation of iron-sulfur proteins in plastids. J Biol Inorg Chem 23(4):545–566
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
Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantaphylidès C, Havaux M (2012) Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc Natl Acad Sci U S A 109:5535–5540
Ramel F, Ksas B, Akkari E, Mialoundama AS, Monnet F, Krieger-Liszkay A, Ravanat JL, Mueller MJ, Bouvier F, Havaux M (2013a) Light-induced acclimation of the Arabidopsis chlorina1 mutant to singlet oxygen. Plant Cell 25:1445–1462
Ramel F, Mialoundama AS, Havaux M (2013b) Nonenzymatic carotenoid oxidation and photooxidative stress signalling in plants. J Exp Bot 64:799–805
Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37
Reichenbächer D, Börner T, Richter J (1978) Untersuchungen am Fraktion-I-Protein der Gerste mit Hilfe quantitativer Immunelektrophoresen. Biochem Physiol Pflanz 172:53–60
Reiss T, Bergfeld R, Link G, Thien W, Mohr H (1983) Photooxidative destruction of chloroplasts and its consequences for cytosolic enzyme levels and plant development. Planta 159:518–528
Ren Y, Li Y, Jiang Y, Wu B, Miao Y (2017) Phosphorylation of WHIRLY1 by CIPK14 shifts its localization and dual functions in Arabidopsis. Mol Plant 10:749–763
Rochaix JD (2013a) Plant science. Fine-tuning photosynthesis. Science 342:50–51
Rochaix JD (2013b) Redox regulation of thylakoid protein kinases and photosynthetic gene expression. Antioxid Redox Signal 18:2184–2201
Rokov-Plavec J, Dulic M, Duchêne AM, Weygand-Durasevic I (2008) Dual targeting of organellar seryl-tRNA synthetase to maize mitochondria and chloroplasts. Plant Cell Rep 27:1157–1168
Rossel JB, Walter PB, Hendrickson L, Chow WS, Poole A, Mullineaux PM, Poson BJ (2006) A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance. Plant Cell Environ 29:269–281
Schmid J, Amrhein N (1995) Molecular organization of the shikimate pathway in higher plants. Phytochemistry 39:737–749
Schuster C, Oelmüller R, Bergfeld R, Mohr H (1988) Recovery of plastids from photooxidative damage: significance of a plastidic factor. Planta 174:289–297
Seguel A, Jelenska J, Herrera-Vásquez A, Marr SK, Joyce MB, Gagesch KR, Shakoor N, Jiang S-C, Fonseca A, Wildermuth MC, Greenberg JT, Holuigue L (2018) PROHIBITIN3 forms complexes with ISOCHORISMATE SYNTHASE1 to regulate stress-induced salicylic acid biosynthesis in Arabidopsis. Plant Physiol 176:2515–2531
Serrano M, Wang B, Aryal B, Garcion C, Abou-Mansour E, Heck S, Geisler M, Mauch F, Nawrath C, Métraux JP (2013) Export of salicylic acid from the chloroplast requires the multidrug and toxin extrusion-like transporter EDS5. Plant Physiol 162:1815–1821
Serrano I, Audran C, Rivas S (2016) Chloroplasts at work during plant innate immunity. J Exp Bot 67:3845–3854
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. Plant J 32:631–639
Sherameti I, Sopory SK, Trebicka A, Pfannschmidt T, Oelmuller R (2002b) Photosynthetic electron transport determines nitrate reductase gene expression and activity in higher plants. J Biol Chem 277:46594–46600
Shine MB, Yang JW, El-Habbak M, Nagyabhyru P, Fu DQ, Navarre D, Ghabrial S, Kachroo P, Kachroo A (2016) Cooperative functioning between phenylalanine ammonia lyase and isochorismate synthase activities contributes to salicylic acid biosynthesis in soybean. New Phytol 212:627–636
Strand Å, Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421:79–83
Strawn MA, Marr SK, Inoue K, Inada N, Zubieta C, Wildermuth MC (2007) Arabidopsis isochorismate synthase functional in pathogen-induced salicylate biosynthesis exhibits properties consistent with a role in diverse stress responses. J Biol Chem 282:5919–5933
Sun X, Feng P, Xu X, Guo H, Ma J, Chi W, Lin R, Lu C, Zhang (2011) A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nat Commun 2:477
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
Szechyńska-Hebda M, Karpiński S (2013) Light intensity-dependent retrograde signalling in higher plants. J Plant Physiol 170:1501–1516
Tadini L, Pesaresi P, Kleine T, Rossi F, Guljamow A, Sommer F, Mühlhaus T, Schroda M, Masiero S, Pribil M, Rothbart M, Hedtke B, Grimm B, Leister D (2016) GUN1 controls accumulation of the plastid ribosomal protein S1 at the protein level and interacts with proteins involved in plastid protein homeostasis. Plant Physiol 170:1817–1830
Tamoi M, Shigeoka S (2015) Diversity of regulatory mechanisms of photosynthetic carbon metabolism in plants and algae. Biosci Biotechnol Biochem 79:870–876
Taylor WC (1989) Regulatory interactions between nuclear and plastid genomes. Annu Rev Plan Physiol Plant Mol Biol 40:211–233
Terasawa K, Sato N (2009) Plastid localization of the PEND protein is mediated by a noncanonical transit peptide. FEBS J 276:1709–1719
Thomas J, Weinstein JD (1990) Measurement of heme efflux and heme content in isolated developing chloroplasts. Plant Physiol 94:1414–1423
Tikkanen M, Gollan PJ, Suorsa M, Kangasjärvi S, Aro EM (2012) STN7 operates in retrograde signaling through controlling redox balance in the electron transfer chain. Front Plant Sci 3:277
Tiller N, Bock R (2014) The translational apparatus of plastids and its role in plant development. Mol Plant 7:1105–1120
Tripathy BC, Sherameti I, Oelmüller R (2010) Siroheme: an essential component for life on earth. Plant Signal Behav 5:14–20
Van Aken O, Pogson BJ (2017) Convergence of mitochondrial and chloroplastic ANAC017/PAP-dependent retrograde signalling pathways and suppression of programmed cell death. Cell Death Differ 24:955–960
van Dijk EL, Chen CL, D’Aubenton-Carafa Y, Gourvennec S, Kwapisz M, Roche V, Bertrand C, Silvain M, Legoix-Né P, Loeillet S (2011) XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature 475:114–117
Van Dingenen J, Blomme J, Gonzalez N, Inze D (2016) Plants grow with a little help from their organelle friends. J Exp Bot 67:6267–6281
Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206
Vranova E, Coman D, Gruissem W (2013) Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol 64:665–700
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
Walley JW, Xiao Y, Wang JZ, Baidoo EE, Keasling JD, Shen Z, Briggs SP, Dehesh K (2015) Plastid-produced interorgannellar stress signal MEcPP potentiates induction of the unfolded protein response in endoplasmic reticulum. Proc Natl Acad Sci U S A 112:6212–6217
Wang L, Kim C, Xu X, Piskurewicz U, Dogra V, Singh S, Mahler H, Apel K (2016) Singlet oxygen- and EXECUTER1-mediated signaling is initiated in grana margins and depends on the protease FtsH2. Proc Natl Acad Sci U S A 113:E3792–E3800
Wang K, Guo Q, Froehlich JE, Hersh HL, Zienkiewicz A, Howe GA, Benning C (2018) Two abscisic acid responsive plastid lipase genes involved in jasmonic acid biosynthesis in Arabidopsis thaliana. Plant Cell 29:1678–1696
Wasternack C, Song S (2017) Jasmonates: biosynthesis, metabolism and signaling by proteins activating and repressing transcription. J Exp Bot 68:1303–1321
Waters MT, Wang P, Korkaric M, Capper RG, Saunders NJ, Langdale JA (2009) GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 21:1109–1128
Weber AP (2004) Solute transporters as connecting elements between cytosol and plastid stroma. Curr Opin Plant Biol 7:247–253
Weber AP, Fischer K (2007) Making the connections – the crucial role of metabolite transporters at the interface between chloroplast and cytosol. FEBS Lett 581:2215–2222
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
Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565
Wilson PB, Estavillo GM, Field KJ, Pornsiriwong W, Carroll AJ, Howell KA, Woo NS, Lake JA, Smith SM, Harvey Millar A, von Caemmerer S, Pogson BJ (2009) The nucleotidase/phosphatase SAL1 is a negative regulator of drought tolerance in Arabidopsis. Plant J 58:299–317
Woodson JD (2016) Chloroplast quality control – balancing energy production and stress. New Phytol 212:36–41
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
Woodson JD, Perez-Ruiz JM, Schmitz RJ, Ecker JR, Chory J (2013) Sigma factor-mediated plastid retrograde signals control nuclear gene expression. Plant J 73:1–13
Xiao Y, Savchenko T, Baidoo EE, Chehab WE, Hayden DM, Tolstikov V, Corwin JA, Kliebenstein DJ, Keasling JD, Dehesh K (2012) Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell 149:1525–1535
Xiao Y, Wang J, Dehesh K (2013) Review of stress specific organelles-to-nucleus metabolic signal molecules in plants. Plant Sci 212:102–107
Xiong JY, Lai CX, Qu Z, Yang XY, Qin XH, Liu GQ (2009) Recruitment of AtWHY1 and AtWHY3 by a distal element upstream of the kinesin gene AtKP1 to mediate transcriptional repression. Plant Mol Biol 71:437–449
Yamasaki K, Motomura Y, Yagi Y, Nomura H, Kikuchi S, Nakai M, Shiina T (2013) Chloroplast envelope localization of EDS5, an essential factor for salicylic acid biosynthesis in Arabidopsis thaliana. Plant Signal Behav 8:e23603
Yoo HH, Kwon C, Lee MM, Chung IK (2007) Single-stranded DNA binding factor AtWHY1 modulates telomere length homeostasis in Arabidopsis. Plant J 49:442–451
Zhang K, Halitschke R, Yin C, Liu CJ, Gan SS (2013) Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism. Proc Natl Acad Sci U S A 110:14807–14812
Zhang L, Zhang F, Melotto M, Yao J, He SY (2017) Jasmonate signaling and manipulation by pathogens and insects. J Exp Bot 68:1371–1385
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Pfalz, J., Oelmüller, R. (2019). Plastid Retrograde Signals: More to Discover. In: Sopory, S. (eds) Sensory Biology of Plants. Springer, Singapore. https://doi.org/10.1007/978-981-13-8922-1_18
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