Abstract
Modern ideas on the nature and functions of plastid retrograde signals, i.e., plastid retrograde signaling, predominantly of chloroplasts, are summarized. The main attention is focused on the participation of plastid retrograde signals in inter- and intracellular signaling pathways and their role in the processes of plant growth and development. The small amount of data on the little-studied retrograde signaling system of plant mitochondria are outlined as well.
Similar content being viewed by others
REFERENCES
Szechyńska-Hebda, M. and Karpiński, S., Light intensity-dependent retrograde signalling in higher plants, J. Plant Physiol., 2013, vol. 170, pp. 1501–1516.
Leister, D., Wang, L., and Kleine, T., Organellar gene expression and acclimation of plants to environmental stress, Front. Plant Sci., 2017, vol. 8: 387.
De Barajas-López, J.D., Blanco, N.E., and Strand, Å., Plastid-to-nucleus communication, signals controlling the running of the plant cell, Biochim. Biophys. Acta, 2013, vol. 1833, pp. 425–437.
Sun, A.Z. and Guo, F.Q., Chloroplast retrograde regulation of heat stress responses in plants, Front. Plant Sci., 2016, vol. 7: 398.
Chi, W., Feng, P., Ma, J., and Zhang, L., Metabolites and chloroplast retrograde signaling, Curr. Opin. Plant Biol., 2015, vol. 25, pp. 32–38.
Chan, K.X., Phua, S.Y., Crisp, P., McQuinn, R., and Pogson, B.J., Learning the languages of the chloroplast: retrograde signaling and beyond, Annu. Rev. Plant Biol., 2016, vol. 67, pp. 25–53.
Van Aken, O. and Pogson, B.J., Convergence of mitochondrial and chloroplastic ANAC017/PAP-dependent retrograde signalling pathways and suppression of programmed cell death, Cell Death Differ., 2017, vol. 24, pp. 955–960.
Chi, W., Sun, X., and Zhang, L., Intracellular signaling from plastid to nucleus, Annu. Rev. Plant Biol., 2013, vol. 64, pp. 559–582.
Börner, T., The discovery of plastid-to-nucleus retrograde signaling—a personal perspective, Protoplasma, 2017, vol. 254, pp. 1845–1855.
Page, M.T., McCormac, A.C., Smith, A.G., and Terry, M.J., Singlet oxygen initiates a plastid signal controlling photosynthetic gene expression, New Phytol., 2017, vol. 213, pp. 1168–1180.
Yurina, N.P. and Odintsova, M.S., Plant signaling systems. Plastid-generated signals and their role in nuclear gene expression, Russ. J. Plant Physiol., 2007, vol. 54, pp. 427–438.
Xiao, Y., Wang, J., and Dehesh, K., Review of stress specific organelles-to-nucleus metabolic signal molecules in plants, Plant Sci., 2013, vol. 212, pp. 102–107.
Singh, R., Singh, S., Parihar, P., Singh, V.P., and Prasad, S.M., Retrograde signaling between plastid and nucleus: a review, J. Plant Physiol., 2015, vol. 181, pp. 55–66.
Kleine, T. and Leister, D., Retrograde signaling: organelles go networking, Biochim. Biophys. Acta, 2016, vol. 1857, pp. 1313–1325.
De Souza, A., Wang, J.Z., and Dehesh, K., Retrograde signals: integrators of interorganellar communication and orchestrators of plant development, Annu. Rev. Plant Biol., 2017, vol. 68, pp. 85–108.
Dietzel, L., Gläßer, C., Liebers, M., Hiekel, S., Courtois, F., Czarnecki, O., Schlicke, H., Zubo, Y., Börner, T., Mayer, K., Grimm, B., and Pfannschmidt, T., Identification of early nuclear target genes of plastidial redox signals that trigger the long-term response of Arabidopsis to light quality shifts, Mol. Plant, 2015, vol. 8, pp. 1237–1252.
Bobik, K. and Burch-Smith, T.M., Chloroplast signaling within, between and beyond cells, Front. Plant Sci., 2015, vol. 6: 781.
Zhang, Z.W., Zhang, G.C., Zhu, F., Zhang, D.W., and Yuan, S., The roles of tetrapyrroles in plastid retrograde signaling and tolerance to environmental stresses, Planta, 2015, vol. 242, pp. 1263–1276.
Karpinska, B., Alomrani, S.O., and Foyer, C.H., Inhibitor-induced oxidation of the nucleus and cytosol in Arabidopsis thaliana: implications for organelle to nucleus retrograde signaling, Philos. Trans. R. Soc. Lond. B Biol. Sci., 2017, vol. 372: 20160392. https://doi.org/10.1098/rstb.2016.0392
Foyer, C.H., Ruban, A.V., and Noctor, G., Viewing oxidative stress through the lens of oxidative signalling rather than damage, Biochem. J., 2017, vol. 474, pp. 877–883.
Rossi, F.R., Krapp, A.R., Bisaro, F., Maiale, S.J., Pieckenstain, F.L., and Carrillo, N., Reactive oxygen species generated in chloroplasts contribute to tobacco leaf infection by the necrotrophic fungus Botrytis cinerea, Plant J., 2017, vol. 92, pp. 761–773.
Kreslavski, V.D., Los, D.A., Allakhverdiev, S.I., and Kuznetsov, Vl.V., Signaling role of reactive oxygen species in plants under stress, Russ. J. Plant Physiol., 2012, vol. 59, pp. 141–154.
Sinetova, M.A. and Los, D.A., Systemic analysis of stress transcriptomics of Synechocystis reveals common stress genes and their universal triggers, Mol. BioSyst., 2016, vol. 12, pp. 3254–3258.
Erickson, J.L., Kantek, M., and Schattat, M.H., Plastid–nucleus distance alters the behavior of stromules, Front. Plant Sci., 2017, vol. 8: 1135.
Whalley, H.J. and Knight, M.R., Calcium signatures are decoded by plants to give specific gene responses, New Phytol., 2013, vol. 197, pp. 690–693.
Kmiecik, P., Leonardelli, M., and Teige, M., Novel connections in plant organellar signalling link different stress responses and signalling pathways, J. Exp. Bot., 2016, vol. 67, pp. 3793–3807.
Gollan, P.J., Tikkanen, M., and Aro, E.M., Photosynthetic light reactions: integral to chloroplast retrograde signaling, Curr. Opin. Plant Biol., 2015, vol. 27, pp. 180–191.
Guo, H., Feng, P., Chi, W., Sun, X., Xu, X., Li, Y., Ren, D., Lu, C., Rochaix, J.D., Leister, D., and Zhang, L., Plastid–nucleus communication involves calcium-modulated MAPK signaling, Nat. Commun., 2016, vol. 7: 12173.
Colombo, M., Tadini, L., Peracchio, C., Ferrari, R., and Pesaresi, P., GUN1, a jack-of-all-trades in chloroplast protein homeostasis and signaling, Front. Plant Sci., 2016, vol. 7: 1427.
Wu, G.Z., Chalvin, C., Hoelscherb, M., Meyer, E.H., Wu, X.N., and Bocka, R., Control of retrograde signaling by rapid turnover of GENOMES UNCOUPLED1, Plant Physiol., 2018, vol. 176, pp. 2472–2495.
Sun, X., Feng, P., Xu, X., Guo, H., Ma, J., Chi, W., Lin, R., Lu, C., and Zhang, L., A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus, Nat. Commun., 2011, vol. 2: 477.
Adam, Z., Plastid intramembrane proteolysis, Biochim. Biophys. Acta, 2015, vol. 1847, pp. 910–914.
Hirosawa, Y., Ito-Inaba, Y., and Inaba, T., Ubiquitin-proteasome-dependent regulation of bidirectional communication between plastids and the nucleus, Front. Plant Sci., 2017, vol. 8: 310.
Tokumaru, M., Adachi, F., Toda, M., Ito-Inaba, Y., Yazu, F., Hirosawa, Y., Sakakibara, Y., Suiko, M., Kakizaki, T., and Inaba, T., Ubiquitin-proteasome dependent regulation of the GOLDEN2-LIKE 1 transcription factor in response to plastid signals, Plant Physiol., 2017, vol. 173, pp. 524–535.
Martín, G., Leivar, P., Ludevid, D., Tepperman, J., Quail, P.H., and Monte, E., Phytochrome and retrograde signalling pathways converge to antagonistically regulate a light-induced transcriptional network, Nat. Commun., 2016, vol. 7: 11431.
Tang, X., Miao, M., Niu, X., Zhang, D., Cao, X., Jin, X., Zhu, Y., Fan, Y., Wang, H., Liu, Y., Sui, Y., Wang, W., Wang, A., Xiao, F., Giovannoni, J., and Liu, Y., Ubiquitin-conjugated degradation of golden 2‑like transcription factor is mediated by CUL4-DDB1-based E3 ligase complex in tomato, New Phytol., 2016, vol. 209, pp. 1028–1039.
Cookson, P.J., Kiano, J.W., Shipton, C.A., Fraser, P.D., Romer, S., Schuch, W., Bramley, P.M., and Pyke, K.A., Increases in cell elongation, plastid compartment size and phytoene synthase activity underlie the phenotype of the high pigment-1 mutant of tomato, Planta, 2003, vol. 217, pp. 896–903.
Huang, D., Lin, W., Deng, B., Ren, Y., and Miao, Y., Dual-located WHIRLY1 interacting with LHCA1 alters photochemical activities of photosystem I and is involved in light adaptation in Arabidopsis, Int. J. Mol. Sci., 2017, vol. 18: 2352.
Ren, Y., Li, Y., Jiang, Y., Wu, B., and Miao, Y., Phosphorylation of WHIRLY1 by CIPK14 shifts its localization and dual functions in Arabidopsis, Mol. Plant, 2017, vol. 10, pp. 749–763.
Kucharewicz, W., Distelfeld, A., Bilger, W., Müller, M., Munné-Bosch, S., Hensel, G., and Krupinska, K., Acceleration of leaf senescence is slowed down in transgenic barley plants deficient in the DNA/RNA-binding protein WHIRLY1, J. Exp. Bot., 2017, vol. 68, pp. 983–996.
Yurina, N.P., Sharapova, L.S., and Odintsova, M.S., Structure of plastid genomes of photosynthetic eukaryotes, Biochemistry (Moscow), 2017, vol. 82, pp. 678–691.
Feng, P., Guo, H., Chi, W., Chai, X., Sun, X., Xu, X., Ma, J., Rochaix, J.D., Leister, D., Wang, H., Lu, C., and Zhang, L., Chloroplast retrograde signal regulates flowering, Proc. Natl. Acad. Sci. USA, 2016, vol. 113, pp. 10708–10713.
Funding
The present work was prepared with the partial financial support of the program of the Presidium of the Russian Academy of Sciences no. 18 Molecular and Cell Biology and Postgenome Technologies of the Russian Foundation for Basic Research (grants no. 16-04-01626 and 19-04-00798) and a Ministry of Science and Higher Education of the Russian Federation.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.
Additional information
Translated by I. Andreev
Abbreviations: ABA—abscisic acid; CAS—Ca2+-binding protein of chloroplasts; β-CC—β-cyclocitral; ER—endoplasmic reticulum; ET—ethylene; ETC—electron transport chain; JA—jasmonate acid; MEcPP—methyleritrolcyclodiphosphate; PAP—phosphoadenosine-5-phosphate; PPR—pentatricopeptide repeat; ROS—reactive oxygen species; RS—retrograde signal; RSG—retrograde signaling; SA—salicylic acid; SU—subunit; TF—transcriptional factor.
Rights and permissions
About this article
Cite this article
Yurina, N.P., Odintsova, M.S. Chloroplast Retrograde Signaling System. Russ J Plant Physiol 66, 509–520 (2019). https://doi.org/10.1134/S1021443719040149
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1021443719040149