1932

Abstract

The chloroplast can act as an environmental sensor, communicating with the cell during biogenesis and operation to change the expression of thousands of proteins. This process, termed retrograde signaling, regulates expression in response to developmental cues and stresses that affect photosynthesis and yield. Recent advances have identified many signals and pathways—including carotenoid derivatives, isoprenes, phosphoadenosines, tetrapyrroles, and heme, together with reactive oxygen species and proteins—that build a communication network to regulate gene expression, RNA turnover, and splicing. However, retrograde signaling pathways have been viewed largely as a means of bilateral communication between organelles and nuclei, ignoring their potential to interact with hormone signaling and the cell as a whole to regulate plant form and function. Here, we discuss new findings on the processes by which organelle communication is initiated, transmitted, and perceived, not only to regulate chloroplastic processes but also to intersect with cellular signaling and alter physiological responses.

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2016-04-29
2024-04-23
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Literature Cited

  1. Adhikari ND, Froehlich JE, Strand DD, Buck SM, Kramer DM, Larkin RM. 1.  2011. GUN4-porphyrin complexes bind the ChlH/GUN5 subunit of Mg-Chelatase and promote chlorophyll biosynthesis in Arabidopsis. Plant Cell 23:1449–67 [Google Scholar]
  2. Ahlfors R, Lång S, Overmyer K, Jaspers P, Brosché M. 2.  et al. 2004. Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses. Plant Cell 16:1925–37 [Google Scholar]
  3. Albrecht V, Simková K, Carrie C, Delannoy E, Giraud E. 3.  et al. 2010. The cytoskeleton and the peroxisomal-targeted SNOWY COTYLEDON3 protein are required for chloroplast development in Arabidopsis. Plant Cell 22:3423–38 [Google Scholar]
  4. Ankele E, Kindgren P, Pesquet E, Strand A. 4.  2007. In vivo visualization of Mg-ProtoporphyrinIX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast. Plant Cell 19:1964–79 [Google Scholar]
  5. Avendaño-Vázquez A-O, Cordoba E, Llamas E, San Román C, Nisar N. 5.  et al. 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 26:2524–37Provides evidence that apocarotenoid signals regulate leaf development and retrograde signaling in a carotenoid biosynthesis mutant. [Google Scholar]
  6. Barajas-López JDD, Kremnev D, Shaikhali J, Piñas-Fernández A, Strand A. 6.  2013. PAPP5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development. PLOS ONE 8:e60305 [Google Scholar]
  7. Barkan A, Small I. 7.  2014. Pentatricopeptide repeat proteins in plants. Annu. Rev. Plant Biol. 65:415–42 [Google Scholar]
  8. Bellafiore S, Barneche F, Peltier G, Rochaix J-D. 8.  2005. State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–95 [Google Scholar]
  9. Blanco NE, Guinea-Díaz M, Whelan J, Strand Å. 9.  2014. Interaction between plastid and mitochondrial retrograde signalling pathways during changes to plastid redox status. Philos. Trans. R. Soc. Lond. B 369:20130231Provides evidence that CDKE1 integrates chloroplast and mitochondrial stress retrograde signals in the nucleus. [Google Scholar]
  10. Bradbeer JW, Atkinson YE, Borner T, Hagemann R. 10.  1979. Cytoplasmic synthesis of plastid polypeptides may be controlled by plastid-synthesized RNA. Nature 279:816–17 [Google Scholar]
  11. Brautigam K, Dietzel L, Kleine T, Stroher E, Wormuth D. 11.  et al. 2009. Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis. Plant Cell 21:2715–32 [Google Scholar]
  12. Brunkard JO, Runkel AM, Zambryski PC. 12.  2015. Chloroplasts extend stromules independently and in response to internal redox signals. PNAS 112:10044–49 [Google Scholar]
  13. Chan KX, Crisp PA, Estavillo GM, Pogson BJ. 13.  2010. Chloroplast-to-nucleus communication: current knowledge, experimental strategies and relationship to drought stress signaling. Plant Signal. Behav. 5:1575–82 [Google Scholar]
  14. Chan KX, Wirtz M, Phua SY, Estavillo GM, Pogson BJ. 14.  2013. Balancing metabolites in drought: the sulfur assimilation conundrum. Trends Plant Sci. 18:18–29 [Google Scholar]
  15. Chen H, Xiong L. 15.  2011. Genetic interaction of two abscisic acid signaling regulators, HY5 and FIERY1, in mediating lateral root formation. Plant Signal. Behav. 6:123–25 [Google Scholar]
  16. Chen H, Zhang B, Hicks LM, Xiong L. 16.  2011. A nucleotide metabolite controls stress-responsive gene expression and plant development. PLOS ONE 6:e26661 [Google Scholar]
  17. Chen S, Kim C, Lee JM, Lee H-A, Fei Z. 17.  et al. 2015. Blocking the QB-binding site of photosystem II by tenuazonic acid, a non-host-specific toxin of Alternaria alternata, activates singlet oxygen-mediated and EXECUTER-dependent signalling in Arabidopsis. Plant Cell Environ. 38:1069–80 [Google Scholar]
  18. Chi W, Sun XW, Zhang LX. 18.  2013. Intracellular signaling from plastid to nucleus. Annu. Rev. Plant Biol. 64:559–82 [Google Scholar]
  19. Chiba Y, Mineta K, Hirai MY, Suzuki Y, Kanaya S. 19.  et al. 2013. Changes in mRNA stability associated with cold stress in Arabidopsis cells. Plant Cell Physiol. 54:180–94 [Google Scholar]
  20. Cottage A, Mott EK, Kempster JA, Gray JC. 20.  2010. The Arabidopsis plastid-signalling mutant gun1 (genomes uncoupled1) shows altered sensitivity to sucrose and abscisic acid and alterations in early seedling development. J. Exp. Bot. 61:3773–86 [Google Scholar]
  21. Czarnecki O, Gläßer C, Chen J-G, Mayer KFX, Grimm B. 21.  2012. Evidence for a contribution of ALA synthesis to plastid-to-nucleus signaling. Front. Plant Sci. 3:236 [Google Scholar]
  22. Desveaux D, Subramaniam R, Després C, Mess J-N, Lévesque C. 22.  et al. 2004. A “Whirly” transcription factor is required for salicylic acid-dependent disease resistance in Arabidopsis. Dev. Cell 6:229–40 [Google Scholar]
  23. Dichtl B, Stevens A, Tollervey D. 23.  1997. Lithium toxicity in yeast is due to the inhibition of RNA processing enzymes. EMBO J. 16:7184–95 [Google Scholar]
  24. Dietz K-J. 24.  2015. Efficient high light acclimation involves rapid processes at multiple mechanistic levels. J. Exp. Bot. 66:2401–14 [Google Scholar]
  25. Dietzel L, Gläßer C, Liebers M, Hiekel S, Courtois F. 25.  et al. 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 8:1237–52 [Google Scholar]
  26. Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D. 26.  et al. 2011. Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012Demonstrates that SAL1-PAP and XRN function in operational retrograde signaling during drought and high light. [Google Scholar]
  27. Fantini E, Falcone G, Frusciante S, Giliberto L, Giuliano G. 27.  2013. Dissection of tomato lycopene biosynthesis through virus-induced gene silencing. Plant Physiol. 163:986–98 [Google Scholar]
  28. Fey V, Wagner R, Brautigam K, Wirtz M, Hell R. 28.  et al. 2005. Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J. Biol. Chem. 280:5318–28 [Google Scholar]
  29. Fischer BB, Krieger-Liszkay A, Hideg E, Snyrychová I, Wiesendanger M, Eggen RIL. 29.  2007. Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii. FEBS Lett. 581:5555–60 [Google Scholar]
  30. Fischer BB, Ledford HK, Wakao S, Huang SG, Casero D. 30.  et al. 2012. SINGLET OXYGEN RESISTANT 1 links reactive electrophile signaling to singlet oxygen acclimation in Chlamydomonas reinhardtii. PNAS 109:E1302–11 [Google Scholar]
  31. Foyer CH, Karpinska B, Krupinska K. 31.  2014. The functions of WHIRLY1 and REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis. Philos. Trans. R. Soc. Lond. B 369:20130226 [Google Scholar]
  32. Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN. 32.  et al. 2006. Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141:436–45 [Google Scholar]
  33. Galvez-Valdivieso G, Fryer MJ, Lawson T, Slattery K, Truman W. 33.  et al. 2009. The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. Plant Cell 21:2143–62 [Google Scholar]
  34. Gigolashvili T, Geier M, Ashykhmina N, Frerigmann H, Wulfert S. 34.  et al. 2012. The Arabidopsis thylakoid ADP/ATP carrier TAAC has an additional role in supplying plastidic phosphoadenosine 5′-phosphosulfate to the cytosol. Plant Cell 24:4187–204 [Google Scholar]
  35. Giraud E, Van Aken O, Ho LHM, Whelan J. 35.  2009. The transcription factor ABI4 is a regulator of mitochondrial retrograde expression of ALTERNATIVE OXIDASE1a. Plant Physiol. 150:1286–96 [Google Scholar]
  36. Gläßer C, Haberer G, Finkemeier I, Pfannschmidt T, Kleine T. 36.  et al. 2014. Meta-analysis of retrograde signaling in Arabidopsis thaliana reveals a core module of genes embedded in complex cellular signaling networks. Mol. Plant 7:1167–90 [Google Scholar]
  37. Gonzalez-Perez S, Gutierrez J, Garcia-Garcia F, Osuna D, Dopazo J. 37.  et al. 2011. Early transcriptional defense responses in Arabidopsis cell suspension culture under high-light conditions. Plant Physiol. 156:1439–56 [Google Scholar]
  38. Grabowski E, Miao Y, Mulisch M, Krupinska K. 38.  2008. Single-stranded DNA-binding protein Whirly1 in barley leaves is located in plastids and the nucleus of the same cell. Plant Physiol. 147:1800–4 [Google Scholar]
  39. Grondin A, Rodrigues O, Verdoucq L, Merlot S, Leonhardt N, Maurel C. 39.  2015. Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. Plant Cell 27:1945–54 [Google Scholar]
  40. Gy I, Gasciolli V, Lauressergues D, Morel J-B, Gombert J. 40.  et al. 2007. Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 19:3451–61 [Google Scholar]
  41. Hanson MR, Sattarzadeh A. 41.  2011. Stromules: recent insights into a long neglected feature of plastid morphology and function. Plant Physiol. 155:1486–92 [Google Scholar]
  42. Häusler RE, Heinrichs L, Schmitz J, Flügge U-I. 42.  2014. How sugars might coordinate chloroplast and nuclear gene expression during acclimation to high light intensities. Mol. Plant 7:1121–37 [Google Scholar]
  43. Havaux M. 43.  2014. Carotenoid oxidation products as stress signals in plants. Plant J. 79:597–606 [Google Scholar]
  44. Hiltscher H, Rudnik R, Shaikhali J, Heiber I, Mellenthin M. 44.  et al. 2014. The radical induced cell death protein 1 (RCD1) supports transcriptional activation of genes for chloroplast antioxidant enzymes. Front. Plant Sci. 5:475 [Google Scholar]
  45. Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K. 45.  2003. Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-l-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J. 33:651–63 [Google Scholar]
  46. Hirsch J, Misson J, Crisp PA, David P, Bayle V. 46.  et al. 2011. A novel fry1 allele reveals the existence of a mutant phenotype unrelated to 5′ to 3′ exoribonuclease (XRN) activities in Arabidopsis thaliana roots. PLOS ONE 6:e16724 [Google Scholar]
  47. Hu Z, Xu F, Guan L, Qian P, Liu Y. 47.  et al. 2014. The tetratricopeptide repeat-containing protein slow green1 is required for chloroplast development in Arabidopsis. J. Exp. Bot. 65:1111–23 [Google Scholar]
  48. Ilg A, Bruno M, Beyer P, Al-Babili S. 48.  2014. Tomato carotenoid cleavage dioxygenases 1A and 1B: Relaxed double bond specificity leads to a plenitude of dialdehydes, mono-apocarotenoids and isoprenoid volatiles. FEBS Open Bio 4:584–93 [Google Scholar]
  49. Isemer R, Krause K, Grabe N, Kitahata N, Asami T, Krupinska K. 49.  2012. Plastid located WHIRLY1 enhances the responsiveness of Arabidopsis seedlings toward abscisic acid. Front. Plant Sci. 3:283 [Google Scholar]
  50. Isemer R, Mulisch M, Schafer A, Kirchner S, Koop H-U, Krupinska K. 50.  2012. Recombinant Whirly1 translocates from transplastomic chloroplasts to the nucleus. FEBS Lett. 586:85–88 [Google Scholar]
  51. Jarvis P, López-Juez E. 51.  2013. Biogenesis and homeostasis of chloroplasts and other plastids. Nat. Rev. Mol. Cell Biol. 14:787–802 [Google Scholar]
  52. Jost R, Altschmied L, Bloem E, Bogs J, Gershenzon J. 52.  et al. 2005. Expression profiling of metabolic genes in response to methyl jasmonate reveals regulation of genes of primary and secondary sulfur-related pathways in Arabidopsis thaliana. Photosynth. Res. 86:491–508 [Google Scholar]
  53. Jung H-S, Crisp PA, Estavillo GM, Cole B, Hong F. 53.  et al. 2013. Subset of heat-shock transcription factors required for the early response of Arabidopsis to excess light. PNAS 110:14474–79 [Google Scholar]
  54. Kachanovsky DE, Filler S, Isaacson T, Hirschberg J. 54.  2012. Epistasis in tomato color mutations involves regulation of phytoene synthase 1 expression by cis-carotenoids. PNAS 109:19021–26 [Google Scholar]
  55. Kakizaki T, Matsumura H, Nakayama K, Che F-S, Terauchi R, Inaba T. 55.  2009. Coordination of plastid protein import and nuclear gene expression by plastid-to-nucleus retrograde signaling. Plant Physiol. 151:1339–53 [Google Scholar]
  56. Kakizaki T, Yazu F, Nakayama K, Ito-Inaba Y, Inaba T. 56.  2011. Plastid signalling under multiple conditions is accompanied by a common defect in RNA editing in plastids. J. Exp. Bot. 63:251–60 [Google Scholar]
  57. Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM. 57.  1997. Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9:627–40 [Google Scholar]
  58. Kato Y, Miura E, Matsushima R, Sakamoto W. 58.  2007. White leaf sectors in yellow variegated2 are formed by viable cells with undifferentiated plastids. Plant Physiol. 144:952–60 [Google Scholar]
  59. Kim B-H, von Arnim AG. 59.  2009. FIERY1 regulates light-mediated repression of cell elongation and flowering time via its 3′(2′),5′-bisphosphate nucleotidase activity. Plant J. 58:208–19 [Google Scholar]
  60. Kim C, Apel K. 60.  2013. 1O2-mediated and EXECUTER-dependent retrograde plastid-to-nucleus signaling in norflurazon-treated seedlings of Arabidopsis thaliana. Mol. Plant 6:1580–91 [Google Scholar]
  61. Kim C, Apel K. 61.  2013. Singlet oxygen-mediated signaling in plants: Moving from flu to wild type reveals an increasing complexity. Photosynth. Res. 116:455–64 [Google Scholar]
  62. Kim C, Meskauskiene R, Zhang S, Lee KP, Lakshmanan Ashok M. 62.  et al. 2012. Chloroplasts of Arabidopsis are the source and a primary target of a plant-specific programmed cell death signaling pathway. Plant Cell 24:3026–39Demonstrates the separation between EX and β-cyclocitral in 1O2-responsive signaling and regulation of SORGs. [Google Scholar]
  63. Kim S, Schlicke H, Van Ree K, Karvonen K, Subramaniam A. 63.  et al. 2013. Arabidopsis chlorophyll biosynthesis: an essential balance between the methylerythritol phosphate and tetrapyrrole pathways. Plant Cell 25:4984–93 [Google Scholar]
  64. Kindgren P, Eriksson M-J, Benedict C, Mohapatra A, Gough SP. 64.  et al. 2011. A novel proteomic approach reveals a role for Mg-protoporphyrin IX in response to oxidative stress. Physiol. Plant. 141:310–20 [Google Scholar]
  65. Kindgren P, Kremnev D, Blanco NE, Barajas López JDD, Fernandez AP. 65.  et al. 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. 70:279–91 [Google Scholar]
  66. Kindgren P, Noren L, Barajas López JDD, Shaikhali J, Strand A. 66.  2012. Interplay between HEAT SHOCK PROTEIN 90 and HY5 controls PhANG expression in response to the GUN5 plastid signal. Mol. Plant 5:901–13 [Google Scholar]
  67. Kopriva S. 67.  2013. 12-oxo-phytodienoic acid interaction with cyclophilin CYP20-3 is a benchmark for understanding retrograde signaling in plants. PNAS 110:9197–98 [Google Scholar]
  68. Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G. 68.  et al. 2007. Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–19 [Google Scholar]
  69. Larkin RM, Alonso JM, Ecker JR, Chory J. 69.  2003. GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299:902–6 [Google Scholar]
  70. Lee B-R, Huseby S, Koprivova A, Chételat A, Wirtz M. 70.  et al. 2012. Effects of fou8/fry1 mutation on sulfur metabolism: Is decreased internal sulfate the trigger of sulfate starvation response?. PLOS ONE 7:e39425 [Google Scholar]
  71. Lee J, He K, Stolc V, Lee H, Figueroa P. 71.  et al. 2007. Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19:731–49 [Google Scholar]
  72. Lee KP, Kim C, Landgraf F, Apel K. 72.  2007. EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. PNAS 104:10270–75 [Google Scholar]
  73. Lepage E, Zampini E, Brisson N. 73.  2013. Plastid genome instability leads to reactive oxygen species production and plastid-to-nucleus retrograde signaling in Arabidopsis. Plant Physiol. 163:867–81 [Google Scholar]
  74. Lepistö A, Toivola J, Nikkanen L, Rintamäki E. 74.  2012. Retrograde signalling from functionally heterogeneous plastids. Front. Plant Sci. 3:286 [Google Scholar]
  75. Li W, Liu B, Yu L, Feng D, Wang H, Wang J. 75.  2009. Phylogenetic analysis, structural evolution and functional divergence of the 12-oxo-phytodienoate acid reductase gene family in plants. BMC Evol. Biol. 9:90 [Google Scholar]
  76. Lv F, Zhou J, Zeng L, Xing D. 76.  2015. β-Cyclocitral upregulates salicylic acid signalling to enhance excess light acclimation in Arabidopsis.. J. Exp. Bot. 66:4719–32 [Google Scholar]
  77. Manmathan H, Shaner D, Snelling J, Tisserat N, Lapitan N. 77.  2013. Virus-induced gene silencing of Arabidopsis thaliana gene homologues in wheat identifies genes conferring improved drought tolerance. J. Exp. Bot. 64:1381–92 [Google Scholar]
  78. Maruyama-Nakashita A, Inoue E, Watanabe-Takahashi A, Yamaya T, Takahashi H. 78.  2003. Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol. 132:597–605 [Google Scholar]
  79. Mathur S, Vyas S, Kapoor S, Tyagi AK. 79.  2011. The Mediator complex in plants: structure, phylogeny, and expression profiling of representative genes in a dicot (Arabidopsis) and a monocot (rice) during reproduction and abiotic stress. Plant Physiol. 157:1609–27 [Google Scholar]
  80. McQuinn RP, Giovannoni JJ, Pogson BJ. 80.  2015. More than meets the eye: from carotenoid biosynthesis, to new insights into apocarotenoid signaling. Curr. Opin. Plant Biol. 27:172–79 [Google Scholar]
  81. Mehrshahi P, Stefano G, Andaloro JM, Brandizzi F, Froehlich JE, DellaPenna D. 81.  2013. Transorganellar complementation redefines the biochemical continuity of endoplasmic reticulum and chloroplasts. PNAS 110:12126–31 [Google Scholar]
  82. Merret R, Descombin J, Juan Y-T, Favory J-J, Carpentier M-C. 82.  et al. 2013. XRN4 and LARP1 are required for a heat-triggered mRNA decay pathway involved in plant acclimation and survival during thermal stress. Cell Rep. 5:1279–93 [Google Scholar]
  83. Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J. 83.  2001. Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. PNAS 98:2053–58 [Google Scholar]
  84. Mochizuki N, Tanaka R, Grimm B, Masuda T, Moulin M. 84.  et al. 2010. The cell biology of tetrapyrroles: a life and death struggle. Trends Plant Sci. 15:488–98 [Google Scholar]
  85. Mochizuki N, Tanaka R, Tanaka A, Masuda T, Nagatani A. 85.  2008. The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis. PNAS 105:15184–89 [Google Scholar]
  86. Moellering ER, Muthan B, Benning C. 86.  2010. Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330:226–28 [Google Scholar]
  87. Moulin M, McCormac AC, Terry MJ, Smith AG. 87.  2008. Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. PNAS 105:15178–83 [Google Scholar]
  88. Müller-Xing R, Xing Q, Goodrich J. 88.  2014. Footprints of the sun: memory of UV and light stress in plants. Front. Plant Sci. 5:474 [Google Scholar]
  89. Muthuramalingam M, Matros A, Scheibe R, Mock HP, Dietz KJ. 89.  2013. The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo. Front. Plant Sci. 4:54 [Google Scholar]
  90. Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R. 90.  2003. Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J. 33:633–50 [Google Scholar]
  91. Oelze M-L, Muthuramalingam M, Vogel MO, Dietz K-J. 91.  2014. The link between transcript regulation and de novo protein synthesis in the retrograde high light acclimation response of Arabidopsis thaliana. BMC Genom. 15:320 [Google Scholar]
  92. Oikawa K, Matsunaga S, Mano S, Kondo M, Yamada K. 92.  et al. 2015. Physical interaction between peroxisomes and chloroplasts elucidated by in situ laser analysis. Nat. Plants 1:15035 [Google Scholar]
  93. Olmedo G, Guo H, Gregory BD, Nourizadeh SD, Aguilar-Henonin L. 93.  et al. 2006. ETHYLENE-INSENSITIVE5 encodes a 5′ to 3′ exoribonuclease required for regulation of the EIN3-targeting F-box proteins EBF1/2. PNAS 103:13286–93 [Google Scholar]
  94. op den Camp RGL, Przybyla D, Ochsenbein C, Laloi C, Kim CH. 94.  et al. 2003. Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–32 [Google Scholar]
  95. Ostrovsky D, Diomina G, Lysak E, Matveeva E, Ogrel O, Trutko S. 95.  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 [Google Scholar]
  96. Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C. 96.  et al. 2000. Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12:1849–62 [Google Scholar]
  97. Park S-W, Li W, Viehhauser A, He B, Kim S. 97.  et al. 2013. Cyclophilin 20-3 relays a 12-oxo-phytodienoic acid signal during stress responsive regulation of cellular redox homeostasis. PNAS 110:9559–64 [Google Scholar]
  98. Pesaresi P, Hertle A, Pribil M, Kleine T, Wagner R. 98.  et al. 2009. Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21:2402–23 [Google Scholar]
  99. Pesaresi P, Masiero S, Eubel H, Braun H-P, Bhushan S. 99.  et al. 2006. Nuclear photosynthetic gene expression is synergistically modulated by rates of protein synthesis in chloroplasts and mitochondria. Plant Cell 18:970–91 [Google Scholar]
  100. Pesaresi P, Mizzotti C, Colombo M, Masiero S. 100.  2014. Genetic regulation and structural changes during tomato fruit development and ripening. Front. Plant Sci. 5:124 [Google Scholar]
  101. Petrillo E, Godoy Herz MA, Fuchs A, Reifer D, Fuller J. 101.  et al. 2014. A chloroplast retrograde signal regulates nuclear alternative splicing. Science 344:427–30Demonstrates PQ redox retrograde signaling in posttranscriptional regulation (alternative splicing) via an unknown systemic signal. [Google Scholar]
  102. Petrov VD, Van Breusegem F. 102.  2012. Hydrogen peroxide—a central hub for information flow in plant cells. AoB Plants 2012:pls014 [Google Scholar]
  103. Pfannschmidt T. 103.  2010. Plastidial retrograde signalling—a true “plastid factor” or just metabolite signatures?. Trends Plant Sci. 15:427–35 [Google Scholar]
  104. Pogson BJ, Woo NS, Forster B, Small ID. 104.  2008. Plastid signalling to the nucleus and beyond. Trends Plant Sci. 13:602–9 [Google Scholar]
  105. Potuschak T, Vansiri A, Binder BM, Lechner E, Vierstra RD, Genschik P. 105.  2006. The exoribonuclease XRN4 is a component of the ethylene response pathway in Arabidopsis. Plant Cell 18:3047–57 [Google Scholar]
  106. Quintero FJ, Garciadeblás B, Rodríguez-Navarro A. 106.  1996. The SAL1 gene of Arabidopsis, encoding an enzyme with 3′(2′),5′-bisphosphate nucleotidase and inositol polyphosphate 1-phosphatase activities, increases salt tolerance in yeast. Plant Cell 8:529–37 [Google Scholar]
  107. Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantaphylides C, Havaux M. 107.  2012. Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. PNAS 109:5535–40Demonstrates sensing and transduction of chloroplast 1O2 signaling via a volatile β-carotene oxidation product. [Google Scholar]
  108. Ramel F, Ksas B, Akkari E, Mialoundama AS, Monnet F. 108.  et al. 2013. Light-induced acclimation of the Arabidopsis chlorina1 mutant to singlet oxygen. Plant Cell 25:1445–62 [Google Scholar]
  109. Rapp JC, Mullet JE. 109.  1991. Chloroplast transcription is required to express the nuclear genes rbcS and cab. Plastid DNA copy number is regulated independently. Plant Mol. Biol. 17:813–23 [Google Scholar]
  110. Riaño-Pachón DM, Corrêa LGG, Trejos-Espinosa R, Mueller-Roeber B. 110.  2008. Green transcription factors: a Chlamydomonas overview. Genetics 179:31–39 [Google Scholar]
  111. Rizhsky L, Liang H, Mittler R. 111.  2003. The water-water cycle is essential for chloroplast protection in the absence of stress. J. Biol. Chem. 278:38921–25 [Google Scholar]
  112. Robles P, Fleury D, Candela H, Cnops G, Alonso-Peral MM. 112.  et al. 2010. The RON1/FRY1/SAL1 gene is required for leaf morphogenesis and venation patterning in Arabidopsis. Plant Physiol. 152:1357–72 [Google Scholar]
  113. Rodríguez VM, Chételat A, Majcherczyk P, Farmer EE. 113.  2010. Chloroplastic phosphoadenosine phosphosulfate metabolism regulates basal levels of the prohormone jasmonic acid in Arabidopsis leaves. Plant Physiol. 152:1335–45 [Google Scholar]
  114. Rodríguez-Concepción M. 114.  2006. Early steps in isoprenoid biosynthesis: multilevel regulation of the supply of common precursors in plant cells. Phytochem. Rev. 5:1–15 [Google Scholar]
  115. Rolland F, Baena-Gonzalez E, Sheen J. 115.  2006. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57:675–709 [Google Scholar]
  116. Rossel JB, Walter PB, Hendrickson L, Chow WS, Poole A. 116.  et al. 2006. A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance. Plant Cell Environ. 29:269–81 [Google Scholar]
  117. Rossel JB, Wilson IW, Pogson BJ. 117.  2002. Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol. 130:1109–20 [Google Scholar]
  118. Rossel JB, Wilson PB, Hussain D, Woo NS, Gordon MJ. 118.  et al. 2007. Systemic and intracellular responses to photooxidative stress in Arabidopsis. Plant Cell 19:4091–110 [Google Scholar]
  119. Ruckle ME, DeMarco SM, Larkin RM. 119.  2007. Plastid signals remodel light signaling networks and are essential for efficient chloroplast biogenesis in Arabidopsis. Plant Cell 19:3944–60 [Google Scholar]
  120. Ruckle ME, Larkin RM. 120.  2009. Plastid signals that affect photomorphogenesis in Arabidopsis thaliana are dependent on GENOMES UNCOUPLED 1 and cryptochrome 1. New Phytol. 182:367–79 [Google Scholar]
  121. Ryu JS, Kim J-I, Kunkel T, Kim BC, Cho DS. 121.  et al. 2005. Phytochrome-specific type 5 phosphatase controls light signal flux by enhancing phytochrome stability and affinity for a signal transducer. Cell 120:395–406 [Google Scholar]
  122. Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F. 122.  et al. 2005. Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J. 44:653–68 [Google Scholar]
  123. Scarpeci TE, Zanor MI, Carrillo N, Mueller-Roeber B, Valle EM. 123.  2008. Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes. Plant Mol. Biol. 66:361–78 [Google Scholar]
  124. Schlicke H, Hartwig AS, Firtzlaff V, Richter AS, Glässer C. 124.  et al. 2014. Induced deactivation of genes encoding chlorophyll biosynthesis enzymes disentangles tetrapyrrole-mediated retrograde signaling. Mol. Plant 7:1211–27 [Google Scholar]
  125. Schwarzländer M, Fricker MD, Sweetlove LJ. 125.  2009. Monitoring the in vivo redox state of plant mitochondria: effect of respiratory inhibitors, abiotic stress and assessment of recovery from oxidative challenge. Biochim. Biophys. Acta 1787:468–75 [Google Scholar]
  126. Schweer J, Türkeri H, Kolpack A, Link G. 126.  2010. Role and regulation of plastid sigma factors and their functional interactors during chloroplast transcription—recent lessons from Arabidopsis thaliana. Eur. J. Cell Biol. 89:940–46 [Google Scholar]
  127. Sewelam N, Jaspert N, Van Der Kelen K, Tognetti VB, Schmitz J. 127.  et al. 2014. Spatial H2O2 signaling specificity: H2O2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially. Mol. Plant 7:1191–210 [Google Scholar]
  128. Shao N, Duan GY, Bock R. 128.  2013. A mediator of singlet oxygen responses in Chlamydomonas reinhardtii and Arabidopsis identified by a luciferase-based genetic screen in algal cells. Plant Cell 25:4209–26 [Google Scholar]
  129. Shumbe L, Bott R, Havaux M. 129.  2014. Dihydroactinidiolide, a high light-induced β-carotene derivative that can regulate gene expression and photoacclimation in Arabidopsis. Mol. Plant 7:1248–51 [Google Scholar]
  130. Simkin AJ, Schwartz SH, Auldridge M, Taylor MG, Klee HJ. 130.  2004. The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles β-ionone, pseudoionone, and geranylacetone. Plant J. 40:882–92 [Google Scholar]
  131. Šimková K, Kim C, Gacek K, Baruah A, Laloi C, Apel K. 131.  2012. The chloroplast division mutant caa33 of Arabidopsis thaliana reveals the crucial impact of chloroplast homeostasis on stress acclimation and retrograde plastid-to-nucleus signaling. Plant J. 69:701–12 [Google Scholar]
  132. Šimková K, Moreau F, Pawlak P, Vriet C, Baruah A. 132.  et al. 2012. Integration of stress-related and reactive oxygen species-mediated signals by Topoisomerase VI in Arabidopsis thaliana. PNAS 109:16360–65 [Google Scholar]
  133. Strand A, Asami T, Alonso J, Ecker JR, Chory J. 133.  2003. Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421:79–83 [Google Scholar]
  134. Strand DD, Livingston AK, Satoh-Cruz M, Froehlich JE, Maurino VG, Kramer DM. 134.  2015. Activation of cyclic electron flow by hydrogen peroxide in vivo. PNAS 112:5539–44 [Google Scholar]
  135. Sullivan J, Gray J. 135.  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 11:901–10 [Google Scholar]
  136. Sun X, Feng P, Xu X, Guo H, Ma J. 136.  et al. 2011. A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nat. Commun. 2:477Provides a mechanism for signal transduction between plastid-localized GUN1 and nuclear ABI4. [Google Scholar]
  137. Susek RE, Ausubel FM, Chory J. 137.  1993. Signal-transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74:787–99 [Google Scholar]
  138. Szechyńska-Hebda M, Karpiński S. 138.  2013. Light intensity-dependent retrograde signalling in higher plants. J. Plant Physiol. 170:1501–16 [Google Scholar]
  139. Tadini L, Romani I, Pribil M, Jahns P, Leister D, Pesaresi P. 139.  2012. Thylakoid redox signals are integrated into organellar-gene-expression-dependent retrograde signaling in the prors1-1 mutant. Front. Plant Sci. 3:282 [Google Scholar]
  140. Takahashi H, Kopriva S, Giordano M, Saito K, Hell R. 140.  2011. Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 62:157–84 [Google Scholar]
  141. Tameshige T, Fujita H, Watanabe K, Toyokura K, Kondo M. 141.  et al. 2013. Pattern dynamics in adaxial-abaxial specific gene expression are modulated by a plastid retrograde signal during Arabidopsis thaliana leaf development. PLOS Genet. 9:e1003655 [Google Scholar]
  142. Terashima I, Hanba YT, Tholen D, Niinemets Ü. 142.  2011. Leaf functional anatomy in relation to photosynthesis. Plant Physiol. 155:108–16 [Google Scholar]
  143. Terry MJ, Smith AG. 143.  2013. A model for tetrapyrrole synthesis as the primary mechanism for plastid-to-nucleus signaling during chloroplast biogenesis. Front. Plant Sci. 4:14 [Google Scholar]
  144. Thomas J, Weinstein JD. 144.  1990. Measurement of heme efflux and heme content in isolated developing chloroplasts. Plant Physiol. 94:1414–23 [Google Scholar]
  145. Tikkanen M, Gollan PJ, Suorsa M, Kangasjärvi S, Aro E-M. 145.  2012. STN7 operates in retrograde signaling through controlling redox balance in the electron transfer chain. Front. Plant Sci. 3:277 [Google Scholar]
  146. Tognetti VB, Muohlenbock P, Van Breusegem F. 146.  2012. Stress homeostasis—the redox and auxin perspective. Plant Cell Environ. 35:321–33 [Google Scholar]
  147. Uberegui E, Hall M, Lorenzo Ó, Schröder WP, Balsera M. 147.  2015. An Arabidopsis soluble chloroplast proteomic analysis reveals the participation of the Executer pathway in response to increased light conditions. J. Exp. Bot. 66:2067–77 [Google Scholar]
  148. Van Aken O, Whelan J. 148.  2012. Comparison of transcriptional changes to chloroplast and mitochondrial perturbations reveals common and specific responses in Arabidopsis. Front. Plant Sci. 3:281 [Google Scholar]
  149. van Dijk EL, Chen CL, d'Aubenton-Carafa Y, Gourvennec S, Kwapisz M. 149.  et al. 2011. XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature 475:114–17 [Google Scholar]
  150. Van Norman JM, Zhang J, Cazzonelli CI, Pogson BJ, Harrison PJ. 150.  et al. 2014. Periodic root branching in Arabidopsis requires synthesis of an uncharacterized carotenoid derivative. PNAS 111:E1300–9 [Google Scholar]
  151. Vogel MO, Moore M, König K, Pecher P, Alsharafa K. 151.  et al. 2014. Fast retrograde signaling in response to high light involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF transcription factors in Arabidopsis. Plant Cell 26:1151–65Provides evidence for a rapid sugar-based retrograde signaling pathway and for the temporal nature of retrograde signals. [Google Scholar]
  152. von Gromoff ED, Alawady A, Meinecke L, Grimm B, Beck CF. 152.  2008. Heme, a plastid-derived regulator of nuclear gene expression in Chlamydomonas. Plant Cell 20:552–67 [Google Scholar]
  153. Wakao S, Chin BL, Ledford HK, Dent RM, Casero D. 153.  et al. 2014. Phosphoprotein SAK1 is a regulator of acclimation to singlet oxygen in Chlamydomonas reinhardtii. eLife 3:e02286 [Google Scholar]
  154. Walley J, Xiao Y, Wang J-Z, Baidoo EE, Keasling JD. 154.  et al. 2015. Plastid-produced interorgannellar stress signal MEcPP potentiates induction of the unfolded protein response in endoplasmic reticulum. PNAS 112:6212–17 [Google Scholar]
  155. Waters MT, Wang P, Korkaric M, Capper RG, Saunders NJ, Langdale JA. 155.  2009. GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 21:1109–28 [Google Scholar]
  156. Wilson PB, Estavillo GM, Field KJ, Pornsiriwong W, Carroll AJ. 156.  et al. 2009. The nucleotidase/phosphatase SAL1 is a negative regulator of drought tolerance in Arabidopsis. Plant J. 58:299–317 [Google Scholar]
  157. Woodson JD, Perez-Ruiz JM, Chory J. 157.  2011. Heme synthesis by plastid ferrochelatase I regulates nuclear gene expression in plants. Curr. Biol. 21:897–903Provides evidence that heme is a positive signal regulating PhANG expression. [Google Scholar]
  158. Woodson JD, Perez-Ruiz JM, Schmitz RJ, Ecker JR, Chory J. 158.  2013. Sigma factor-mediated plastid retrograde signals control nuclear gene expression. Plant J. 73:1–13 [Google Scholar]
  159. Xiao Y, Savchenko T, Baidoo EEK, Chehab WE, Hayden DM. 159.  et al. 2012. Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell 149:1525–35Provides evidence that the isoprenoid precusor MEcPP functions in retrograde signaling, SA biosynthesis, and stress responses. [Google Scholar]
  160. Xiong L, Lee B, Ishitani M, Lee H, Zhang C, Zhu JK. 160.  2001. FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev. 15:1971–84 [Google Scholar]
  161. Yoshida K, Igarashi E, Mukai M, Hirata K, Miyamoto K. 161.  2003. Induction of tolerance to oxidative stress in the green alga, Chlamydomonas reinhardtii, by abscisic acid. Plant Cell Environ. 26:451–57 [Google Scholar]
  162. Zhang J, Vanneste S, Brewer PB, Michniewicz M, Grones P. 162.  et al. 2011. Inositol trisphosphate-induced Ca2+ signaling modulates auxin transport and PIN polarity. Dev. Cell 20:855–66 [Google Scholar]
  163. Zhong S, Fei Z, Chen Y-R, Zheng Y, Huang M. 163.  et al. 2013. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat. Biotechnol. 31:154–59 [Google Scholar]
  164. Zhou X, Welsch R, Yang Y, Álvarez D, Riediger M. 164.  et al. 2015. Arabidopsis OR proteins are the major posttranscriptional regulators of phytoene synthase in controlling carotenoid biosynthesis. PNAS 112:3558–63 [Google Scholar]
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