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Biologia Plantarum

, Volume 62, Issue 3, pp 428–438 | Cite as

Gene expression analysis reveals function of TERF1 in plastid-nucleus retrograde signaling under drought stress conditions

  • W. Wu
  • L.-L. Liu
  • T. Yang
  • J.-H. Wang
  • J.-Y. Wang
  • P. Lv
  • Y.-C. Yan
Original paper
  • 128 Downloads

Abstract

Ethylene response factor (ERF) is a key transcription factor of plant ethylene signaling pathway, which plays an important role in plant response to abiotic and biotic stresses by regulating the expression of downstream genes. However, little is known about the mechanisms of the regulation of gene expression by ERF proteins. Chloroplast is an essential organelle that is important for photosynthesis and biosynthesis of many essential metabolites. There exists an interaction between chloroplasts and the nucleus. Chloroplasts can send multiple kinds of signals to regulate the nuclear gene expression known as retrograde signaling. In our study, we have analyzed the expression of the components related to plastid retrograde signaling pathway to elucidate the mechanism of tomato ethylene responsive factor 1 (TERF1) in response to drought stress. Our results showed that TERF1 can regulate different biogenic and operational retrograde signals to regulate nuclear genes expression, which can improve plant tolerance to drought stress. We also propose a new potential of TERF1 in regulating nuclear gene expression, including regulation of different phytohormone signaling pathways and gene posttranscriptional modification triggered by different retrograde signals. Our results have enriched our knowledge about the function of ERF proteins and ethylene signaling pathway.

Additional key words

chloroplast-nucleus interactions ethylene response factor Solanum lycopersicum tomato 

Abbreviations

12-OPDA

12-oxophyto-dienoic acid

ABA

abscisic acid

ABI4

ABA insensitive 4

AOS

allene oxide synthase

CSK

chloroplast sensor kinase

ERF

ethylene response factor

GLK

golden 2-like

GUN

genomes uncoupled

HPL

hydroxyperoxide lyase

JA

jasmonic acid

MBS

methylene blue sensitivity

PAP

3’-phosphoadenosine 5’-phosphate

PEP

plastid-encoded plastid RNA polymerase

PhANGs

photosynthesis-associated nuclear genes

PRANGs

plastid redox-associated nuclear genes

PRIN2

plastid redox insensitive 2

PS

photosystem

ROS

reactive oxygen species

RpoTp

RNA polymerase of the phage T3/T7 type in plastid

RpoTmp

RNA polymerase of the phage T3/T7 type in plastid and mitochondria

SA

salicylic acid

SIG

sigma factors

TERF1

tomato ethylene responsive factor 1

WT

wild-type

XRN

5'-3' exoribonuclease

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Supplementary material

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References

  1. Abdallah, F., Salamini, F., Leister, D.: A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. - Trends Plant Sci. 5: 141–142, 2000.CrossRefPubMedGoogle Scholar
  2. Ankele, E., Kindgren, P., Pesquet, E., Strand, A.: In vivo visualization of Mg-protoporphyrin IX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast. - Plant Cell 19: 1964–1979, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Barajas-Lopez, J. de D., Blanco, N.E., Strand, A.: Plastid-tonucleus communication, signals controlling the running of the plant cell. - Biochim. biophys. Acta 1833: 425–437, 2013.CrossRefGoogle Scholar
  4. Belbin, F.E., Noordally, Z.B., Wetherill, S.J., Atkins, K.A., Franklin, K.A., Dodd, A.N.: Integration of light and circadian signals that regulate chloroplast transcription by a nuclear-encoded sigma factor. - New Phytol. 213: 727–738, 2017.CrossRefPubMedGoogle Scholar
  5. Bellafiore, S., Barneche, F., Peltier, G., Rochaix, J.D.: State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. - Nature 433: 892–895, 2005.CrossRefPubMedGoogle Scholar
  6. Blanco, N.E., Guinea-Diaz, M., Whelan, J., Strand, A.: Interaction between plastid and mitochondrial retrograde signalling pathways during changes to plastid redox status. - Phil. Trans. roy. Soc. London B Biol. Sci. 369: 20130231, 2014.CrossRefGoogle Scholar
  7. Brautigam, K., Dietzel, L., Kleine, T., Stroher, E., Wormuth, D., Dietz, K.J., Radke, D., Wirtz, M., Hell, R., Dormann, P., Nunes-Nesi, A., Schauer, N., Fernie, A.R., Oliver, S.N., Geigenberger, P., Leister, D., Pfannschmidt, T.: Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis. - Plant Cell 21: 2715–2732, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chan, K.X., Phua, S.Y., Crisp, P., McQuinn, R., Pogson, B.J.: Learning the languages of the chloroplast: retrograde signaling and beyond. - Annu. Rev. Plant Biol. 67: 25–53, 2016.CrossRefPubMedGoogle Scholar
  9. Chehab, E.W., Kaspi, R., Savchenko, T., Rowe, H., Negre-Zakharov, F., Kliebenstein, D., Dehesh, K.: Distinct roles of jasmonates and aldehydes in plant-defense responses. - PLoS ONE 3: e1904, 2008.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Chen, H., Zhang, B., Hicks, L.M., Xiong, L.: A nucleotide metabolite controls stress-responsive gene expression and plant development. - PLoS ONE 6: e26661, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Dussault, A., Pouliot, M.: Rapid and simple comparison of messenger RNA levels using real-time PCR. - Biol. Procedures Online 8: 1–10, 2006.CrossRefGoogle Scholar
  12. Estavillo, G.M., Crisp, P.A., Pornsiriwong, W., Wirtz, M., Collinge, D., Carrie, C., Giraud, E., Whelan, J., David, P., Javot, H., Brearley, C, Hell, R., Marin, E., Pogson, B.J.: Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. - Plant Cell 23: 3992–4012, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Fernandez-Pozo, N., Menda, N., Edwards, J.D., Saha, S., Tecle, I.Y., Strickler, S.R., Bombarely, A., Fisher-York, T., Pujar, A., Foerster, H., Yan, A., Mueller, L.A.: The Sol Genomics Network (SGN) — from genotype to phenotype to breeding. - Nucl. Acids Res. 43 (Database Issue): D1036–1041, 2015.CrossRefPubMedGoogle Scholar
  14. Fey, V., Wagner, R., Brautigam, K., Wirtz, M., Hell, R., Dietzmann, A., Leister, D., Oelmuller, R., Pfannschmidt, T.: Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. - J. biol. Chem. 280: 5318–5328, 2005.CrossRefPubMedGoogle Scholar
  15. Foyer, C.H., Kerchev, P.I., Hancock, R.D.: The ABAINSENSITIVE-4 (ABI4) transcription factor links redox, hormone and sugar signaling pathways. - Plant Signal. Behav. 7: 276–281, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Frost, C.J., Mescher, M.C., Dervinis, C., Davis, J.M., Carlson, J.E., De Moraes, C.M.: Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. - New Phytol. 180: 722–734, 2008.CrossRefPubMedGoogle Scholar
  17. Galvez-Valdivieso, G., Fryer, M.J., Lawson, T., Slattery, K., Truman, W., Smirnoff, N., Asami, T., Davies, W.J., Jones, A.M., Baker, N.R., Mullineaux, P.M.: The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. - Plant Cell 21: 2143–2162, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Garapati, P., Xue, G.P., Munne-Bosch, S., Balazadeh, S.: Transcription factor ATAF1 in Arabidopsis promotes senescence by direct regulation of key chloroplast maintenance and senescence transcriptional cascades. - Plant Physiol. 168: 1122–1139, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Geigenberger, P., Thormahlen, I., Daloso, D.M., Fernie, A.R.: The unprecedented versatility of the plant thioredoxin system. - Trends Plant Sci. 22: 249–262, 2017.CrossRefPubMedGoogle Scholar
  20. Glasser, C., Haberer, G., Finkemeier, I., Pfannschmidt, T., Kleine, T., Leister, D., Dietz, K.J., Hausler, R.E., Grimm, B., Mayer, K.F.: Meta-analysis of retrograde signaling in Arabidopsis thaliana reveals a core module of genes embedded in complex cellular signaling networks. - Mol. Plants 7: 1167–1190, 2014.CrossRefGoogle Scholar
  21. Goltsev, V., Yordanov, I., Stoyanova, T., Popov, O.: Hightemperature damage and acclimation of the photosynthetic apparatus: II. Effect of mono- and divalent cations and pH on the temperature sensitivity of some functional characteristics of chloroplasts isolated from heat-acclimated and non-acclimated bean plants. - Planta 170: 478–488, 1987.CrossRefPubMedGoogle Scholar
  22. Grieshaber, N.A., Fischer, E.R., Mead, D.J., Dooley, C.A., Hackstadt, T.: Chlamydial histone-DNA interactions are disrupted by a metabolite in the methylerythritol phosphate pathway of isoprenoid biosynthesis. - Proc. nat. Acad. Sci. USA 101: 7451–7456, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hassidim, M., Yakir, E., Fradkin, D., Hilman, D., Kron, I., Keren, N., Harir, Y., Yerushalmi, S., Green, R.M.: Mutations in chloroplast RNA binding provide evidence for the involvement of the chloroplast in the regulation of the circadian clock in Arabidopsis. - Plant J. 51: 551–562, 2007.CrossRefPubMedGoogle Scholar
  24. Hausler, R.E., Heinrichs, L., Schmitz, J., Flugge, U.I.: How sugars might coordinate chloroplast and nuclear gene expression during acclimation to high light intensities. - Mol. Plants 7: 1121–1137, 2014.CrossRefGoogle Scholar
  25. Hiltscher, H., Rudnik, R., Shaikhali, J., Heiber, I., Mellenthin, M., Meirelles Duarte, I., Schuster, G., Kahmann, U., Baier, M.: The radical induced cell death protein 1 (RCD1) supports transcriptional activation of genes for chloroplast antioxidant enzymes. - Front. Plant Sci. 5: 475–488, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hofgen, R., Willmitzer, L.: Storage of competent cells for Agrobacterium transformation. - Nucl. Acids Res. 16: 9877, 1988.CrossRefPubMedGoogle Scholar
  27. Howell, S.H.: Endoplasmic reticulum stress responses in plants. - Annu. Rev. Plant Biol. 64: 477–499, 2013.CrossRefPubMedGoogle Scholar
  28. Hricova, A., Quesada, V., Micol, J.L.: The SCABRA3 nuclear gene encodes the plastid RpoTp RNA polymerase, which is required for chloroplast biogenesis and mesophyll cell proliferation in Arabidopsis. - Plant Physiol. 141: 942–956, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hu, Z., Xu, F., Guan, L., Qian, P., Liu, Y., Zhang, H., Huang, Y., Hou, S.: The tetratricopeptide repeat-containing protein slow green1 is required for chloroplast development in Arabidopsis. - J. exp. Bot. 65: 1111–1123, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Huang, Z., Zhang, Z., Zhang, X., Zhang, H., Huang, D., Huang, R.: Tomato TERF1 modulates ethylene response and enhances osmotic stress tolerance by activating expression of downstream genes. - FEBS Lett. 573: 110–116, 2004.CrossRefPubMedGoogle Scholar
  31. Iwata, Y., Koizumi, N.: Plant transducers of the endoplasmic reticulum unfolded protein response. - Trends Plant Sci. 17: 720–727, 2012.CrossRefPubMedGoogle Scholar
  32. Kachroo, A., Shanklin, J., Whittle, E., Lapchyk, L., Hildebrand, D., Kachroo, P.: The Arabidopsis stearoyl-acyl carrier protein-desaturase family and the contribution of leaf isoforms to oleic acid synthesis. - Plant mol. Biol. 63: 257–271, 2007.CrossRefPubMedGoogle Scholar
  33. Kakizaki, T., Matsumura, H., Nakayama, K., Che, F.S., Terauchi, R., Inaba, T.: Coordination of plastid protein import and nuclear gene expression by plastid-to-nucleus retrograde signaling. - Plant Physiol. 151: 1339–1353, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kindgren, P., Kremnev, D., Blanco, N.E., De Dios Barajas Lopez, J., Fernandez, A.P., Tellgren-Roth, C., Kleine, T., Small, I., Strand, A.c.: 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, 2012.CrossRefPubMedGoogle Scholar
  35. Kmiecik, P., Leonardelli, M., Teige, M.: Novel connections in plant organellar signalling link different stress responses and signalling pathways. - J. exp. Bot. 67: 3793–3807, 2016.CrossRefPubMedGoogle Scholar
  36. Koussevitzky, S., Nott, A., Mockler, T.C., Hong, F., Sachetto- Martins, G., Surpin, M., Lim, J., Mittler, R., Chory, J.: Signals from chloroplasts converge to regulate nuclear gene expression. - Science 316: 715–719, 2007.CrossRefPubMedGoogle Scholar
  37. Lee, K.P., Kim, C., Landgraf, F., Apel, K.: EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. - Proc. nat. Acad. Sci. USA 104: 10270–10275, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Leister, D., Kleine, T.: Definition of a core module for the nuclear retrograde response to altered organellar gene expression identifies GLK overexpressors as gun mutants. - Physiol. Plant. 157: 297–309, 2016.CrossRefPubMedGoogle Scholar
  39. Liao, W., Li, Y., Yang, Y., Wang, G., Peng, M.: Exposure to various abscission-promoting treatments suggests substantial ERF subfamily transcription factors involvement in the regulation of cassava leaf abscission. - BMC Genomics 17: 538–552, 2016.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lv, F., Zhou, J., Zeng, L., Xing, D.: Beta-cyclocitral upregulates salicylic acid signalling to enhance excess light acclimation in Arabidopsis. - J. exp. Bot. 66: 4719–4732, 2015.CrossRefPubMedGoogle Scholar
  41. Maekawa, S., Takabayashi, A., Huarancca Reyes, T., Yamamoto, H., Tanaka, A., Sato, T., Yamaguchi, J.: Palegreen phenotype of atl31atl6 double mutant leaves is caused by disruption of 5-aminolevulinic acid biosynthesis in Arabidopsis thaliana. - PLoS ONE 10: e0117662, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Maiti, I.B., Murphy, J.F., Shaw, J.G., Hunt, A.G.: Plants that express a potyvirus proteinase gene are resistant to virus infection. - Proc. nat. Acad. Sci. USA 90: 6110–6114, 1993.CrossRefPubMedGoogle Scholar
  43. Mandal, M.K., Chandra-Shekara, A.C., Jeong, R.D., Yu, K., Zhu, S., Chanda, B., Navarre, D., Kachroo A., Kachroo, P.: Oleic acid-dependent modulation of NITRIC OXIDE ASSOCIATED1 protein levels regulates nitric oxidemediated defense signaling in Arabidopsis. - Plant Cell. 24: 1654–1674, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Maruyama, Y., Yamoto, N., Suzuki, Y., Chiba, Y., Yamazaki, K., Sato, T., Yamaguchi, J.: The Arabidopsis transcriptional repressor ERF9 participates in resistance against necrotrophic fungi. - Plant Sci. 213: 79–87, 2013.CrossRefPubMedGoogle Scholar
  45. Mata-Perez, C., Sanchez-Calvo, B., Padilla, M.N., Begara- Morales, J.C., Luque, F., Melguizo, M., Jimenez-Ruiz, J., Fierro-Risco, J., Penas-Sanjuan, A., Valderrama, R., Peñas- Sanjuán, A., Valderrama, R., Corpas, F.J., Barroso, J.B.: Nitro-fatty acids in plant signaling: nitro-linolenic acid induces the molecular chaperone network in Arabidopsis. - Plant Physiol. 170: 686–701, 2016.CrossRefPubMedGoogle Scholar
  46. Merret, R., Descombin, J., Juan, Y.T., Favory, J.J., Carpentier, M.C., Chaparro, C., Charng, Y.Y., Deragon, J.M., Bousquet- Antonelli, C.: XRN4 and LARP1 are required for a heattriggered mRNA decay pathway involved in plant acclimation and survival during thermal stress. - Cell Rep. 5: 1279–1293, 2013.CrossRefPubMedGoogle Scholar
  47. Mochizuki, N., Brusslan, J.A., Larkin, R., Nagatani, A., Chory, J.: Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. - Proc. nat. Acad. Sci. USA 98: 2053–2058, 2001.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Mou, Z., He, Y., Dai, Y., Liu, X., Li, J.: Deficiency in fatty acid synthase leads to premature cell death and dramatic alterations in plant morphology. - Plant Cell 12: 405–418, 2000.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Neuhaus, H.E., Emes, M.J.: Nonphotosynthetic metabolism in plastids. - Annu. Rev. Plant Physiol. Plant mol. Biol. 51: 111–140, 2000.CrossRefPubMedGoogle Scholar
  50. Op den Camp, R.G., Przybyla, D., Ochsenbein, C., Laloi, C., Kim, C., Danon, A., Wagner, D., Hideg, E., Gobel, C., Feussner, I., Nater, M., Apel, K.: Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. - Plant Cell 15: 2320–2332, 2003.CrossRefGoogle Scholar
  51. Page, M.T., Kacprzak, S.M., Mochizuki, N., Okamoto, H., Smith, A.G., Terry, M.J.: Seedlings lacking the PTM protein do not show a genomes uncoupled (gun) mutant phenotype. - Plant Physiol. 174: 21–26, 2017.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Park, S.W., Li, W., Viehhauser, A., He, B., Kim, S., Nilsson, A.K., Andersson, M.X., Kittle, J.D., Ambavaram, M.M., Luan, S., Esker, A.R., Tholl, D., Cimini, D., Ellerström, M., Coaker, G., Mitchell, T.K., Pereira, A., Dietz, K.J., Lawrence, C.B.: Cyclophilin 20-3 relays a 12-oxophytodienoic acid signal during stress responsive regulation of cellular redox homeostasis. - Proc. nat. Acad. Sci. USA 110: 9559–9564, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Pesaresi, P., Masiero, S., Eubel, H., Braun, H.P., Bhushan, S., Glaser, E., Salamini, F., Leister, D.: Nuclear photosynthetic gene expression is synergistically modulated by rates of protein synthesis in chloroplasts and mitochondria. - Plant Cell 18: 970–991, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Pesaresi, P., Varotto, C., Meurer, J., Jahns, P., Salamini, F., Leister, D.: Knock-out of the plastid ribosomal protein L11 in Arabidopsis: effects on mRNA translation and photosynthesis. - Plant J. 27: 179–189, 2001.CrossRefPubMedGoogle Scholar
  55. Puthiyaveetil, S., Ibrahim, I.M., Allen, J.F.: Oxidation-reduction signalling components in regulatory pathways of state transitions and photosystem stoichiometry adjustment in chloroplasts. - Plant Cell Environ. 35: 347–359, 2012.CrossRefPubMedGoogle Scholar
  56. Ramel, F., Ksas, B., Akkari, E., Mialoundama, A.S., Monnet, F., Krieger-Liszkay, A., Ravanat, J.L., Mueller, M.J., Bouvier, F., Havaux, M.: Light-induced acclimation of the Arabidopsis chlorina1 mutant to singlet oxygen. - Plant Cell 25: 1445–1462, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Rauf, M., Arif, M., Dortay, H., Matallana-Ramirez, L.P., Waters, M.T., Gil Nam, H., Lim, P.O., Mueller-Roeber, B., Balazadeh, S.: ORE1 balances leaf senescence against maintenance by antagonizing G2-like-mediated transcription. - EMBO Rep. 14: 382–388, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Robles, P., Fleury, D., Candela, H., Cnops, G., Alonso-Peral, M.M., Anami, S., Falcone, A., Caldana, C., Willmitzer, L., Ponce, M.R., Van Lijsebettens, M., Micol, J.L.: The RON1/FRY1/SAL1 gene is required for leaf morphogenesis and venation patterning in Arabidopsis. - Plant Physiol. 152: 1357–1372, 2010.CrossRefPubMedGoogle Scholar
  59. Rodriguez, V.M., Chetelat, A., Majcherczyk, P., Farmer, E.E.: Chloroplastic phosphoadenosine phosphosulfate metabolism regulates basal levels of the prohormone jasmonic acid in Arabidopsis leaves. - Plant Physiol. 152: 1335–1345, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Rossel, J.B., Walter, P.B., Hendrickson, L., Chow, W.S., Poole, A., Mullineaux, P.M., Pogson, B.J.: 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, 2006.CrossRefPubMedGoogle Scholar
  61. Rossel, J.B., Wilson, P.B., Hussain, D., Woo, N.S., Gordon, M.J., Mewett, O.P., Howell, K.A., Whelan, J., Kazan, K., Pogson, B.J.: Systemic and intracellular responses to photooxidative stress in Arabidopsis. - Plant Cell 19: 4091–4110, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Ruckle, M.E, Larkin, R.M.: Plastid signals that affect photomorphogenesis in Arabidopsis thaliana are dependent on Genomes Uncoupled 1 and Cryptochrome 1. - New Phytol. 182: 367–379, 2009.CrossRefPubMedGoogle Scholar
  63. Savchenko, T., Kolla, V.A., Wang, C.Q., Nasafi, Z., Hicks, D.R., Phadungchob, B., Chehab, W.E., Brandizzi, F., Froehlich, J., Dehesh, K.: Functional convergence of oxylipin and abscisic acid pathways controls stomatal closure in response to drought. - Plant Physiol. 164: 1151–1160, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  64. Schaller, A., Stintzi, A.: Enzymes in jasmonate biosynthesis - structure, function, regulation. - Phytochemistry 70: 1532–1538, 2009.CrossRefPubMedGoogle Scholar
  65. Schlicke, H., Hartwig, A.S., Firtzlaff, V., Richter, A.S., Glasser, C., Maier, K., Finkemeier, I., Grimm, B.: Induced deactivation of genes encoding chlorophyll biosynthesis enzymes disentangles tetrapyrrole-mediated retrograde signaling. - Mol. Plants 7: 1211–1227, 2014.CrossRefGoogle Scholar
  66. Schweer, J., Turkeri, H., Kolpack, A., Link, G.: Role and regulation of plastid sigma factors and their functional interactors during chloroplast transcription — recent lessons from Arabidopsis thaliana. - Eur. J. cel.l Biol. 89: 940–946, 2010.CrossRefGoogle Scholar
  67. Shao, N., Duan, G.Y., Bock, R.: A mediator of singlet oxygen responses in Chlamydomonas reinhardtii and Arabidopsis identified by a luciferase-based genetic screen in algal cells. - Plant Cell 25: 4209–4226, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Shimizu, M., Kato, H., Ogawa, T., Kurachi, A., Nakagawa, Y., Kobayashi, H.: Sigma factor phosphorylation in the photosynthetic control of photosystem stoichiometry. - Proc. nat. Acad. Sci. USA 107: 10760–10764, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Shu, K., Zhang, H., Wang, S., Chen, M., Wu, Y., Tang, S., Liu, C., Feng, Y., Cao, X., Xie, Q.: ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. - PLoS Genet. 9: e1003577, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Shumbe, L., D'Alessandro, S., Shao, N., Chevalier, A., Ksas, B., Bock, R., Havaux, M.: Methylene blue sensitivity 1 (MBS1) is required for acclimation of Arabidopsis to singlet oxygen and acts downstream of beta-cyclocitral. - Plant Cell Environ. 40: 216–226, 2017.CrossRefPubMedGoogle Scholar
  71. Steiner, S., Schroter, Y., Pfalz, J., Pfannschmidt, T.: Identification of essential subunits in the plastid-encoded RNA polymerase complex reveals building blocks for proper plastid development. - Plant Physiol. 157: 1043–1055, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  72. Sun, A.Z., Guo, F.Q.: Chloroplast retrograde regulation of heat stress responses in plants. - Front. Plant Sci. 7: 398–413, 2016.PubMedPubMedCentralGoogle Scholar
  73. Sun, X., Feng, P., Xu, X., Guo, H., Ma, J., Chi, W., Lin, R., Lu, C., Zhang, L.: A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. - Natur. Commun. 2: 477–486, 2011.CrossRefGoogle Scholar
  74. Tadini, L., Romani, I., Pribil, M., Jahns, P., Leister, D., Pesaresi, P.: Thylakoid redox signals are integrated into organellargene- expression-dependent retrograde signaling in the prors1-1 mutant. - Front. Plant Sci. 3: 282–294, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Tameshige, T., Fujita, H., Watanabe, K., Toyokura, K., Kondo, M., Tatematsu, K., Matsumoto, N., Tsugeki, R., Kawaguchi, M., Nishimura, M., Okada, K.: Pattern dynamics in adaxialabaxial specific gene expression are modulated by a plastid retrograde signal during Arabidopsis thaliana leaf development. - PLoS Genet. 9: e1003655, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  76. Thormahlen, I., Meitzel, T., Groysman, J., Ochsner, A.B., Von Roepenack-Lahaye, E., Naranjo, B., Cejudo, F.J., Geigenberger, P.: Thioredoxin f1 and NADPH-dependent thioredoxin reductase C have overlapping functions in regulating photosynthetic metabolism and plant growth in response to varying light conditions. - Plant Physiol. 169: 1766–1786, 2015.PubMedPubMedCentralGoogle Scholar
  77. Tikkanen, M., Gollan, P.J., Suorsa, M., Kangasjarvi, S., Aro, E.M.: STN7 operates in retrograde signaling through controlling redox balance in the electron transfer chain. - Front. Plant Sci. 3: 277–287, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  78. Tognetti, V.B., Muhlenbock, P., Van Breusegem, F.: Stress homeostasis — the redox and auxin perspective. - Plant Cell Environ. 35: 321–333, 2012.CrossRefPubMedGoogle Scholar
  79. VanWijk, K.J., Van Hasselt, P.R.: Photoinhibition of photosystem II in vivo is preceded by down-regulation through light-induced acidification of the lumen: consequences for the mechanism of photoinhibition in vivo. - Planta 189: 359–368, 1993.CrossRefGoogle Scholar
  80. Vogel, M.O., Moore, M., Konig, K., Pecher, P., Alsharafa, K., Lee, J., Dietz, K.J.: Fast retrograde signaling in response to high light involves metabolite export, mitogen-activated proteinkinase 6, and AP2/ERF transcription factors in Arabidopsis. - Plant Cell. 26: 1151–1165, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wan, L., Wu, Y., Huang, J., Dai, X., Lei, Y., Yan, L., Jiang, H., Zhang, J., Varshney, R.K., Liao, B.: Identification of ERF genes in peanuts and functional analysis of AhERF008 and AhERF019 in abiotic stress response. - Funct. integr. Genomics 14: 467–477, 2014.CrossRefPubMedGoogle Scholar
  82. Wang, C., Dehesh, K.: From retrograde signaling to flowering time. - Plant Signal. Behav. 10: e1022012, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  83. Wang, C.Q., Guthrie, C., Sarmast, M.K., Dehesh, K.: BBX19 interacts with CONSTANS to repress FLOWERING LOCUS T transcription, defining a flowering time checkpoint in Arabidopsis. - Plant Cell. 26: 3589–3602, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  84. Wang, C.Q., Sarmast, M.K., Jiang, J., Dehesh, K.: The transcriptional regulator BBX19 promotes hypocotyl growth by facilitating COP1-mediated Early Flowering 3 degradation in Arabidopsis. - Plant Cell 27: 1128–1139, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  85. Waters, M.T., Moylan, E.C., Langdale, J.A.: GLK transcription factors regulate chloroplast development in a cellautonomous manner. - Plant J. 56: 432–444, 2008.CrossRefPubMedGoogle Scholar
  86. Waters, M.T., Wang, P., Korkaric, M., Capper, R.G., Saunders, N.J., Langdale, J.A.: GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. - Plant Cell 21: 1109–1128, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  87. Wilson, M.E., Mixdorf, M., Berg, R.H., Haswell, E.S.: Plastid osmotic stress influences cell differentiation at the plant shoot apex. - Development 143: 3382–3393, 2016.CrossRefPubMedPubMedCentralGoogle Scholar
  88. Wilson, P.B., Estavillo, G.M., Field, K.J., Pornsiriwong, W., Carroll, A.J., Howell, K.A., Woo, N.S., Lake, J.A., Smith, S.M., Harvey Millar, A., Von Caemmerer, S., Pogson, B.J.: The nucleotidase/phosphatase SAL1 is a negative regulator of drought tolerance in Arabidopsis. - Plant J. 58: 299–317, 2009.CrossRefPubMedGoogle Scholar
  89. Woodson, J.D., Chory, J.: Coordination of gene expression between organellar and nuclear genomes. - Nat. Rev. Genet. 9: 383–395, 2008.CrossRefPubMedPubMedCentralGoogle Scholar
  90. Woodson, J.D., Perez-Ruiz, J.M., Chory, J.: Heme synthesis by plastid ferrochelatase I regulates nuclear gene expression in plants. - Curr. Biol. 21: 897–903, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  91. Woodson, J.D., Perez-Ruiz, J.M., Schmitz, R.J., Ecker, J.R., Chory, J.: Sigma factor-mediated plastid retrograde signals control nuclear gene expression. - Plant J. 73: 1–13, 2013.CrossRefPubMedGoogle Scholar
  92. Wu, J., Sun, Y., Zhao, Y., Zhang, J., Luo, L., Li, M., Wang, J., Yu, H., Liu, G., Yang, L., Xiong, G., Zhou, J., Zuo, J., Wang, Y., Li, J.: Deficient plastidic fatty acid synthesis triggers cell death by modulating mitochondrial reactive oxygen species. - Cell Res. 25: 621–633, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  93. Xiao, Y., Savchenko, T., Baidoo, E.E., Chehab, W.E., Hayden, D.M., Tolstikov, V., Corwin, J.A., Kliebenstein, D.J., Keasling, J.D., Dehesh, K.: Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. - Cell 149: 1525–1535, 2012.CrossRefPubMedGoogle Scholar
  94. Xiong, L., Lee, B., Ishitani, M., Lee, H., Zhang, C., Zhu, J.K.: FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. - Genes Dev. 15: 1971–1984, 2001.CrossRefPubMedPubMedCentralGoogle Scholar
  95. Zhang, J., Vanneste, S., Brewer, P.B., Michniewicz, M., Grones, P., Kleine-Vehn, J., Lofke, C., Teichmann, T., Bielach, A., Cannoot, B., Hoyerová, K., Chen, X., Xue, H.W., Benková, E., Zažímalová, E., Friml, J.: Inositol trisphosphate-induced Ca2+ signaling modulates auxin transport and PIN polarity. - Dev. Cell. 20: 855–866, 2011.CrossRefPubMedGoogle Scholar
  96. Zhao, P., Cui, R., Xu, P., Wu, J., Mao, J.L., Chen, Y., Zhou, C.Z., Yu, L.H., Xiang, C.B.: ATHB17 enhances stress tolerance by coordinating photosynthesis associated nuclear gene and ATSIG5 expression in response to abiotic stress. - Sci. Rep. 7: 45492–45506, 2017.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  • W. Wu
    • 1
  • L.-L. Liu
    • 1
  • T. Yang
    • 1
  • J.-H. Wang
    • 1
  • J.-Y. Wang
    • 1
  • P. Lv
    • 1
  • Y.-C. Yan
    • 1
  1. 1.Graduate SchoolChinese Academy of Agricultural SciencesBeijingP.R. China

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