The plastid redox insensitive 2 mutant of Arabidopsis is impaired in PEP activity and high light-dependent plastid redox signalling to the nucleus

Plant Journal

Volumn 70, Issue 2, 2012, Pages 279-291

  Kindgren, Peter ^a,b   Kremnev, Dmitry ^a   Blanco, Nicolás E ^a   De Dios Barajas López, Juan ^a   Fernández, Aurora Piñas ^a   Tellgren Roth, Christian ^c   Small, Ian ^b   Strand, Åsa ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

chloroplast; LHCB; PEP; photosynthesis; redox; signalling

Indexed keywords

ARABIDOPSIS; CHLOROPLAST; CHLOROPLAST GENOME; CURRENT STATUS; FLUORESCENCE RATIO; INTRACELLULAR SIGNALLING; LHCB; NUCLEAR GENE EXPRESSION; NUCLEOIDS; PEP; PHOTOINACTIVATION; PHOTOSYNTHESIS GENES; PHOTOSYNTHETIC APPARATUS; PHOTOSYNTHETIC ELECTRON TRANSPORT; PHOTOSYNTHETIC GENES; PHOTOSYSTEM II; PLASTID-ENCODED RNA POLYMERASE; REDOX; REDOX SIGNALLING; TRANSCRIPTOME ANALYSIS;

CHLOROPHYLL; ELECTRON TRANSITIONS; ELECTRON TRANSPORT PROPERTIES; MACHINERY; PHOTOSYNTHESIS; RNA; SIGNALING;

GENE EXPRESSION;

ARABIDOPSIS PROTEIN; CHLOROPHYLL; DNA DIRECTED RNA POLYMERASE; ISOPROTEIN; PHOTOPROTEIN; PRIN2 PROTEIN, ARABIDOPSIS; SIGNAL PEPTIDE; TETRAPYRROLE DERIVATIVE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CELL NUCLEUS; CHLOROPLAST; CONFOCAL MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; LIGHT; LIGHT HARVESTING SYSTEM; METABOLISM; MOLECULAR GENETICS; MUTATION; OXIDATION REDUCTION REACTION; PLASTID; PROTOPLAST; RADIATION EXPOSURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL NUCLEUS; CHLOROPHYLL; CHLOROPLASTS; DNA-DIRECTED RNA POLYMERASES; GENE EXPRESSION REGULATION, PLANT; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; MUTATION; OXIDATION-REDUCTION; PLASTIDS; PROTEIN ISOFORMS; PROTOPLASTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; TETRAPYRROLES;

ARABIDOPSIS;

EID: 84859498941     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04865.x     Document Type: Article

References (71)

1. Allison, L.A., Simon, L.D., and, Maliga, P., (1996) Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants. EMBO J. 15, 2802-2809. (Pubitemid 26176257)
2. Ankele, E., Kindgren, P., Pesquet, E., and, Strand, A., (2007) In vivo visualization of Mg-protoporphyrin IX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast. Plant Cell, 19 (6), 1964-1979. (Pubitemid 47218852)
3. Arsova, B., Hoja, U., Wimmelbacher, M., Greiner, E., Ustun, S., Melzer, M., Petersen, K., Lein, W., and, Bornke, F., (2010) Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell, 22 (5), 1498-1515.
4. Baginsky, S., Tiller, K., and, Link, G., (1997) Transcription factor phosphorylation by a protein kinase associated with chloroplast RNA polymerase from mustard (Sinapis alba). Plant Mol. Biol. 34 (2), 181-189. (Pubitemid 27268636)
5. Bellafiore, S., Barneche, F., Peltier, G., and, Rochaix, J.D., (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature, 433 (7028), 892-895. (Pubitemid 40314901)
6. Bräutigam, K., Dietzel, L., and, Pfannschmidt, T., (2007) Plastid-nucleus communication: anterograde and retrograde signalling in the development and function of plastids. Cell Mol. Biol. Plastids, 19, 409-455.
7. Chateigner-Boutin, A.L., Ramos-Vega, M., Guevara-Garcia, A., et al. (2008) CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J. 56 (4), 590-602.
8. Chiu, C.C., and, Li, H.M., (2008) Tic40 is important for reinsertion of proteins from the chloroplast stroma into the inner membrane. Plant J. 56 (5), 793-801.
9. Chou, M.L., Fitzpatrick, L.M., Tu, S.L., Budziszewski, G., Potter-Lewis, S., Akita, M., Levin, J.Z., Keegstra, K., and, Li, H.M., (2003) Tic40, a membrane-anchored co-chaperone homolog in the chloroplast protein translocon. EMBO J. 22 (12), 2970-2980. (Pubitemid 36758618)
10. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16 (6), 735-743.
11. DeSantis-Maciossek, G., Kofer, W., Bock, A., Schoch, S., Maier, R.M., Wanner, G., Rudiger, W., Koop, H.U., and, Herrmann, R.G., (1999) Targeted disruption of the plastid RNA polymerase gene rpoA, B and C1: molecular biology, biochemistry and ultrastructure. Plant J. 18, 477-489.
12. Emanuelsson, O., Brunak, S., von Heijne, G., and, Nielsen, H., (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2 (4), 953-971. (Pubitemid 46745592)
13. Escoubas, J.M., Lomas, M., LaRoche, J., and, Falkowski, P.G., (1995) Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc. Natl Acad. Sci. USA, 92 (22), 10237-10241.
14. Fernandez, A.P., and, Strand, A., (2008) Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Curr. Opin. Plant Biol. 11 (5), 509-513.
15. Fey, V., Wagner, R., Brautigam, K., and, Pfannschmidt, T., (2005a) Photosynthetic redox control of nuclear gene expression. J. Exp. Bot. 56 (416), 1491-1498. (Pubitemid 40764438)
16. Fey, V., Wagner, R., Brautigam, K., Wirtz, M., Hell, R., Dietzmann, A., Leister, D., Oelmuller, R., and, Pfannschmidt, T., (2005b) Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J. Biol. Chem. 280 (7), 5318-5328. (Pubitemid 40280005)
17. Gray, G.R., Chauvin, L.P., Sarhan, F., and, Huner, N., (1997) Cold acclimation and freezing tolerance (a complex interaction of light and temperature). Plant Physiol. 114 (2), 467-474. (Pubitemid 28378536)
18. Hajdukiewicz, P.T., Allison, L.A., and, Maliga, P., (1997) The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J. 16 (13), 4041-4048. (Pubitemid 27281019)
19. Hanaoka, M., Kanamaru, K., Takahashi, H., and, Tanaka, K., (2003) Molecular genetic analysis of chloroplast gene promoters dependent on SIG2, a nucleus-encoded sigma factor for the plastid-encoded RNA polymerase, in Arabidopsis thaliana. Nucleic Acids Res. 31 (24), 7090-7098. (Pubitemid 38008442)
20. Hanaoka, M., Kanamaru, K., Fujiwara, M., Takahashi, H., and, Tanaka, K., (2005) Glutamyl-tRNA mediates a switch in RNA polymerase use during chloroplast biogenesis. EMBO Rep. 6 (6), 545-550. (Pubitemid 40973963)
21. Hedtke, B., Borner, T., and, Weihe, A., (1997) Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. Science, 277 (5327), 809-811. (Pubitemid 27366730)
22. Hedtke, B., Borner, T., and, Weihe, A., (2000) One RNA polymerase serving two genomes. EMBO Rep. 1 (5), 435-440.
23. Heiber, I., Stroher, E., Raatz, B., Busse, I., Kahmann, U., Bevan, M.W., Dietz, K.J., and, Baier, M., (2007) The redox imbalanced mutants of Arabidopsis differentiate signaling pathways for redox regulation of chloroplast antioxidant enzymes. Plant Physiol. 143 (4), 1774-1788. (Pubitemid 46849486)
24. Hess, W.R., Muller, A., Nagy, F., and, Borner, T., (1994) Ribosome-deficient plastids affect transcription of light-induced nuclear genes: genetic evidence for a plastid-derived signal. Mol. Gen. Genet. 242 (3), 305-312. (Pubitemid 24061211)
25. Huner, N.P.A., Öquist, G., and, Sarhan, F., (1998) Energy balance and acclimation to light and cold. Trends Plant Sci. 3, 224-230. (Pubitemid 28271169)
26. Karimi, M., Inze, D., and, Depicker, A., (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7 (5), 193-195. (Pubitemid 36725938)
27. Karpinski, S., Gabrys, H., Mateo, A., Karpinska, B., and, Mullineaux, P.M., (2003) Light perception in plant disease defence signalling. Curr. Opin. Plant. Bio. 6, 390-396. (Pubitemid 36964868)
28. Kimura, M., Yamamoto, Y.Y., Seki, M., Sakurai, T., Sato, M., Abe, T., Yoshida, S., Manabe, K., Shinozaki, K., and, Matsui, M., (2003) Identification of Arabidopsis genes regulated by high light-stress using cDNA microarray. Photochem. Photobiol. 77 (2), 226-233.
29. Kinoshita, K., and, Obayashi, T., (2009) Multi-dimensional correlations for gene coexpression and application to the large-scale data of Arabidopsis. Bioinformatics, 25 (20), 2677-2684.
30. Kleine, T., Kindgren, P., Benedict, C., Hendrickson, L., and, Strand, A., (2007) Genome-wide gene expression analysis reveals a critical role for CRYPTOCHROME1 in the response of Arabidopsis to high irradiance. Plant Physiol. 144 (3), 1391-1406. (Pubitemid 47037456)
31. van Kooten, O., and, Snel, J., (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth. Res. 25, 147-150.
32. Koussevitzky, S., Nott, A., Mockler, T.C., Hong, F., Sachetto-Martins, G., Surpin, M., Lim, J., Mittler, R., and, Chory, J., (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science, 316 (5825), 715-719. (Pubitemid 46717673)
33. Larkin, R.M., Alonso, J.M., Ecker, J.R., and, Chory, J., (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science, 299 (5608), 902-906. (Pubitemid 36182451)
34. Lukowitz, W., Gillmor, C.S., and, Scheible, W.R., (2000) Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol. 123 (3), 795-805. (Pubitemid 30466831)
35. Martin, W., Rujan, T., Richly, E., Hansen, A., Cornelsen, S., Lins, T., Leister, D., Stoebe, B., Hasegawa, M., and, Penny, D., (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl Acad. Sci. USA, 99 (19), 12246-12251.
36. Mochizuki, N., Tanaka, R., Tanaka, A., Masuda, T., and, Nagatani, A., (2008) The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis. Proc. Natl Acad. Sci. USA, 105 (39), 15184-15189.
37. Nott, A., Jung, H.S., Koussevitzky, S., and, Chory, J., (2006) Plastid-to-nucleus retrograde signaling. Ann. Rev. Plant Biol. 57, 739-759. (Pubitemid 44061043)
38. Obayashi, T., and, Kinoshita, K., (2009) Rank of correlation coefficient as a comparable measure for biological significance of gene coexpression. DNA Res. 16 (5), 249-260.
39. Oelmuller, R., Levitan, I., Bergfeld, R., Rajasekhar, V., and, Mohr, H., (1986) Expression of nuclear genes is affected by treatments acting on the plastids. Planta, 168, 482-492.
40. Oswald, O., Martin, T., Dominy, P.J., and, Graham, I.A., (2001) Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc. Natl Acad. Sci. USA, 13, 2047-2052. (Pubitemid 32165620)
41. Pfaffl, M.W., (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (9), e45.
42. Pfalz, J., Liere, K., Kandlbinder, A., Dietz, K.J., and, Oelmuller, R., (2006) pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell, 18 (1), 176-197. (Pubitemid 43951323)
43. Pfannschmidt, T., (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci. 8 (1), 33-41. (Pubitemid 36725965)
44. Pfannschmidt, T., and, Liere, K., (2005) Redox regulation and modification of proteins controlling chloroplast gene expression. Antioxid. Redox Signal. 7 (5-6), 607-618. (Pubitemid 40563198)
45. Pfannschmidt, T., and, Link, G., (1994) Separation of two classes of plastid DNA-dependent RNA polymerases that are differentially expressed in mustard (Sinapis alba L.) seedlings. Plant Mol. Biol. 25 (1), 69-81. (Pubitemid 2094085)
46. Pfannschmidt, T., Schutze, K., Brost, M., and, Oelmuller, R., (2001) A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. J. Biol. Chem. 276 (39), 36125-36130.
47. Pogson, B.J., Woo, N.S., Forster, B., and, Small, I.D., (2008) Plastid signalling to the nucleus and beyond. Trends Plant Sci. 13 (11), 602-609.
48. Porra, R.J., Thompson, W.A., and, Kriedemann, P.E., (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta, 975, 384-394.
49. Puthiyaveetil, S., Kavanagh, T.A., Cain, P., Sullivan, J.A., Newell, C.A., Gray, J.C., Robinson, C., van der Giezen, M., Rogers, M.B., and, Allen, J.F., (2008) The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proc. Natl Acad. Sci. USA, 105 (29), 10061-10066.
50. Puthiyaveetil, S., Ibrahim, I.M., Jelicic, B., Tomasic, A., Fulgosi, H., and, Allen, J.F., (2010) Transcriptional control of photosynthesis genes: the evolutionarily conserved regulatory mechanism in plastid genome function. Genome Biol. Evol. 2, 888-896.
51. Ramakers, C., Ruijter, J.M., Deprez, R.H., and, Moorman, A.F., (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339 (1), 62-66. (Pubitemid 36263221)
52. Rapp, J.C., and, Mullet, J.E., (1991) Chloroplast transcription is required to express the nuclear genes rbcS and cab. Plastid DNA copy number is regulated independently. Plant Mol. Biol. 17 (4), 813-823.
53. Reiss, T., and, Link, G., (1985) Characterization of transcriptionally active DNA-protein complexes from chloroplasts and etioplasts of mustard (Sinapis alba L.). Eur. J. Biochem. 148 (2), 207-212.
54. Rodermel, S., (2001) Pathways of plastid-to-nucleus signaling. Trends Plant Sci. 6 (10), 471-478. (Pubitemid 33145955)
55. Rossel, J.B., Wilson, I.W., and, Pogson, B.J., (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol. 130 (3), 1109-1120. (Pubitemid 35352939)
56. Sato, N., Albrieux, C., Joyard, J., Douce, R., and, Kuroiwa, T., (1993) Detection and characterization of a plastid envelope DNA-binding protein which may anchor plastid nucleoids. EMBO J. 12 (2), 555-561. (Pubitemid 23073701)
57. Schroter, Y., Steiner, S., Matthai, K., and, Pfannschmidt, T., (2010) Analysis of oligomeric protein complexes in the chloroplast sub-proteome of nucleic acid-binding proteins from mustard reveals potential redox regulators of plastid gene expression. Proteomics, 10 (11), 2191-2204.
58. Seidel, T., Golldack, D., and, Dietz, K.J., (2005) Mapping of C-termini of V-ATPase subunits by in vivo-FRET measurements. FEBS Lett. 579 (20), 4374-4382. (Pubitemid 41116368)
59. Shimizu, M., Kato, H., Ogawa, T., Kurachi, A., Nakagawa, Y., and, Kobayashi, H., (2010) Sigma factor phosphorylation in the photosynthetic control of photosystem stoichiometry. Proc. Natl Acad. Sci. USA, 107 (23), 10760-10764.
60. Soll, J., and, Schleiff, E., (2004) Protein import into chloroplasts. Nat. Rev. Mol. Cell Biol. 5 (3), 198-208. (Pubitemid 38325801)
61. Steiner, S., Dietzel, L., Schroter, Y., Fey, V., Wagner, R., and, Pfannschmidt, T., (2009) The role of phosphorylation in redox regulation of photosynthesis genes psaA and psbA during photosynthetic acclimation of mustard. Mol. Plant, 2 (3), 416-429.
62. Strand, A., Asami, T., Alonso, J., Ecker, J.R., and, Chory, J., (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature, 421 (6918), 79-83. (Pubitemid 36077088)
63. Suck, R., Zeltz, P., Falk, J., Acker, A., Kossel, H., and, Krupinska, K., (1996) Transcriptionally active chromosomes (TACs) of barley chloroplasts contain the alpha-subunit of plastome-encoded RNA polymerase. Curr. Genet. 30 (6), 515-521. (Pubitemid 27029244)
64. Sullivan, J.A., and, Gray, J.C., (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 (5), 901-910.
65. Susek, R.E., Ausubel, F.M., and, Chory, J., (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell, 74 (5), 787-799. (Pubitemid 23270599)
66. Timmis, J.N., Ayliffe, M.A., Huang, C.Y., and, Martin, W., (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5 (2), 123-135. (Pubitemid 38160279)
67. Vanderauwera, S., Zimmermann, P., Rombauts, S., Vandenabeele, S., Langebartels, C., Gruissem, W., Inze, D., and, Van Breusegem, F., (2005) Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol. 139 (2), 806-821. (Pubitemid 43907108)
68. Wakasugi, T., Tsudzuki, T., and, Sugiura, M., (2001) The genomics of land plant chloroplasts: gene content and alterations of genomic information by RNA editing. Photosynth. Res. 70, 107-118. (Pubitemid 34133281)
69. Zhai, Z., Sooksa-nguan, T., and, Vatamaniuk, O.K., (2009) Establishing RNA interference as a reverse-genetic approach for gene functional analysis in protoplasts. Plant Physiol. 149 (2), 642-652.
70. Zhang, Z.W., Yuan, S., Feng, H., Xu, F., Cheng, J., Shang, J., Zhang, D.W., and, Lin, H.H., (2011) Transient accumulation of Mg-protoporphyrin IX regulates expression of PhANGs-New evidence for the signaling role of tetrapyrroles in mature Arabidopsis plants. J. Plant Physiol. 168 (7), 714-721.
71. Zhou, W., Cheng, Y., Yap, A., Chateigner-Boutin, A.L., Delannoy, E., Hammani, K., Small, I., and, Huang, J., (2009) The Arabidopsis gene YS1 encoding a DYW protein is required for editing of rpoB transcripts and the rapid development of chloroplasts during early growth. Plant J. 58 (1), 82-96.