Identification of four plastid-localized protein kinases

FEBS Letters

Volumn , Issue , 2016, Pages 1749-1756

  Richter, Andreas S ^a   Gartmann, Hans ^a   Fechler, Mona ^a   Rödiger, Anja ^b   Baginsky, Sacha ^b   Grimm, Bernhard ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

chloroplast; post translational control; protein kinase

Indexed keywords

GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTEIN KINASE;

AMINO ACID SEQUENCE; CHLOROPLAST; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; LETTER; MASS SPECTROMETRY; NONHUMAN; PLANT GROWTH; PLANT LEAF; PRIORITY JOURNAL; SEQUENCE ALIGNMENT; SUCROSE DENSITY GRADIENT CENTRIFUGATION; TOBACCO;

EID: 84977533565     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1002/1873-3468.12223     Document Type: Article

References (35)

1. Adams JA (2001) Kinetic and catalytic mechanisms of protein kinases. Chem Rev 101, 2271–2290.
2. van Wijk KJ, Friso G, Walther D and Schulze WX (2014) Meta-analysis of Arabidopsis thaliana phospho-proteomics data reveals compartmentalization of phosphorylation motifs. Plant Cell 26, 2367–2389.
3. Bennett J (1979) Chloroplast phosphoproteins. Phosphorylation of polypeptides of the light-harvesting chlorophyll protein complex. Eur J Biochem 99, 133–137.
4. Reiland S, Messerli G, Baerenfaller K, Gerrits B, Endler A, Grossmann J, Gruissem W and Baginsky S (2009) Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol 150, 889–903.
5. Reiland S, Finazzi G, Endler A, Willig A, Baerenfaller K, Grossmann J, Gerrits B, Rutishauser D, Gruissem W, Rochaix JD et al. (2011) Comparative phosphoproteome profiling reveals a function of the STN8 kinase in fine-tuning of cyclic electron flow (CEF). Proc Natl Acad Sci USA 108, 12955–12960.
6. Schonberg A, Bergner E, Helm S, Agne B, Dunschede B, Schunemann D, Schutkowski M and Baginsky S (2014) The peptide microarray “ChloroPhos1.0” identifies new phosphorylation targets of plastid casein kinase II (pCKII) in Arabidopsis thaliana. PLoS One 9, e108344.
7. Bayer RG, Stael S, Rocha AG, Mair A, Vothknecht UC and Teige M (2012) Chloroplast-localized protein kinases: a step forward towards a complete inventory. J Exp Bot 63, 1713–1723.
8. Schönberg A and Baginsky S (2012) Signal integration by chloroplast phosphorylation networks: an update. Front Plant Sci 3, 256.
9. Baginsky S and Gruissem W (2009) The chloroplast kinase network: new insights from large-scale phosphoproteome profiling. Mol Plant 2, 1141–1153.
10. Baginsky S (2016) Protein phosphorylation in chloroplasts – a survey of phosphorylation targets. J Exp Bot, doi: 10.1093/jxb/erw098.
11. Schliebner I, Pribil M, Zühlke J, Dietzmann A and Leister D (2008) A survey of chloroplast protein kinases and phosphatases in Arabidopsis thaliana. Curr Genomics 9, 184–190.
12. Stael S, Bayer RG, Mehlmer N and Teige M (2011) Protein N-acylation overrides differing targeting signals. FEBS Lett 585, 517–522.
13. Lundquist PK, Davis JI and van Wijk KJ (2012) ABC1K atypical kinases in plants: filling the organellar kinase void. Trends Plant Sci 17, 546–555.
14. Bellafiore S, Barneche F, Peltier G and Rochaix J-D (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433, 892–895.
15. Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, Jahns P and Leister D (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437, 1179–1182.
16. Lu Y, Savage LJ, Larson MD, Wilkerson CG and Last RL (2011) Chloroplast 2010: a database for large-scale phenotypic screening of Arabidopsis mutants. Plant Physiol 155, 1589–1600.
17. Myouga F, Akiyama K, Tomonaga Y, Kato A, Sato Y, Kobayashi M, Nagata N, Sakurai T and Shinozaki K (2013) The Chloroplast Function Database II: a comprehensive collection of homozygous mutants and their phenotypic/genotypic traits for nuclear-encoded chloroplast proteins. Plant Cell Physiol 54, e2.
18. Kuromori T, Wada T, Kamiya A, Yuguchi M, Yokouchi T, Imura Y, Takabe H, Sakurai T, Akiyama K, Hirayama T et al. (2006) A trial of phenome analysis using 4000 Ds-insertional mutants in gene-coding regions of Arabidopsis. Plant J 47, 640–651.
19. Heazlewood JL, Verboom RE, Tonti-Filippini J, Small I and Millar AH (2007) SUBA: the Arabidopsis subcellular database. Nucleic Acids Res 35, D213–D218.
20. Ytterberg AJ, Peltier JB and van Wijk KJ (2006) Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiol 140, 984–997.
21. Larkin RM, Alonso JM, Ecker JR and Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299, 902–906.
22. Peter E and Grimm B (2009) GUN4 is required for posttranslational control of plant tetrapyrrole biosynthesis. Mol Plant 2, 1198–1210.
23. Garcia-Hernandez M, Berardini TZ, Chen G, Crist D, Doyle A, Huala E, Knee E, Lambrecht M, Miller N, Mueller LA et al. (2002) TAIR: a resource for integrated Arabidopsis data. Funct Integr Genomics 2, 239–253.
24. Hanks SK, Quinn AM and Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42–52.
25. Baginsky S, Tiller K, Pfannschmidt T and Link G (1999) PTK, the chloroplast RNA polymerase-associated protein kinase from mustard (Sinapis alba), mediates redox control of plastid in vitro transcription. Plant Mol Biol 39, 1013–1023.
26. Ogrzewalla K, Piotrowski M, Reinbothe S and Link G (2002) The plastid transcription kinase from mustard (Sinapis alba L.). A nuclear-encoded CK2-type chloroplast enzyme with redox-sensitive function. Eur J Biochem 269, 3329–3337.
27. Lu Q, Ding S, Reiland S, Rodiger A, Roschitzki B, Xue P, Gruissem W, Lu C and Baginsky S (2015) Identification and characterization of chloroplast casein kinase II from Oryza sativa (rice). J Exp Bot 66, 175–187.
28. Martinis J, Glauser G, Valimareanu S, Stettler M, Zeeman SC, Yamamoto H, Shikanai T and Kessler F (2014) ABC1K1/PGR6 kinase: a regulatory link between photosynthetic activity and chloroplast metabolism. Plant J 77, 269–283.
29. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV and Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2, e718.
30. Savage LJ, Imre KM, Hall DA and Last RL (2013) Analysis of essential Arabidopsis nuclear genes encoding plastid-targeted proteins. PLoS One 8, e73291.
31. Schonberg A and Baginsky S (2015) The peptide microarray ChloroPhos1.0: a screening tool for the identification of Arabidopsis thaliana chloroplast protein kinase substrates. Methods Mol Biol 1306, 147–157.
32. Chincinska IA, Liesche J, Krugel U, Michalska J, Geigenberger P, Grimm B and Kuhn C (2008) Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiol 146, 515–528.
33. Emanuelsson O, Nielsen H and von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8, 978–984.
34. Kannangara CG, Gough SP, Hansen B, Rasmussen JN and Simpson DJ (1977) Homogenizer with replaceable razor blades for bulk isolation of active barley plastids. Carlsberg Res Commun 42, 431–439.
35. Rodiger A, Agne B, Baerenfaller K and Baginsky S (2014) Arabidopsis proteomics: a simple and standardizable workflow for quantitative proteome characterization. Methods Mol Biol 1072, 275–288.