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Large-scale analysis of protein phosphorylation in Populus leaves

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Abstract

Protein phosphorylation is a key regulatory factor in all aspects of plant biology; most regulatory pathways are governed by the reversible phosphorylation of proteins. To better understand the role that phosphorylated proteins play in a woody model plant, we performed a systemic analysis of the phosphoproteome from Populus leaves using high accuracy NanoLC–MS/MS in combination with biochemical enrichments using strong cation exchange chromatography and titanium dioxide chromatography. We identified 104 phosphopeptides from 94 phosphoproteins and determined 111 phosphorylation sites including 93 occurring on serine residues and 18 on threonine residues. The identified phosphoproteins are involved in a wide variety of metabolic processes. Among these identified phosphoproteins, 68 phosphorylation sites (72 %) were located outside of conserved domains. The identified phosphopeptides share a common phosphorylation motif of pS/pT-P/D-S/A. These data suggest that the Populus metabolism and gene regulation machinery are major targets of phosphorylation. To our knowledge, this is the first gel-free, large-scale phosphoproteomics analysis in woody plants. The identified phosphorylation sites will be a valuable resource for many fields of plant biology, and information gained from the study will provide a better understanding of protein phosphorylation.

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Abbreviations

IMAC:

Immobilized metal affinity

TiO2 :

Titanium dioxide

NanoLC–ESI–MS/MS:

Nano, liquid chromatography-tandem mass spectrometry

References

  • Agrawal GK, Thelen JJ (2006) Large scale identification and quantitative profiling of phosphoproteins expressed during seed filling in oilseed rape. Mol Cell Proteomics 5:2044–2059

    Article  PubMed  CAS  Google Scholar 

  • Baginsky S (2009) Plant proteomics: concepts, applications, and novel strategies for data interpretation. Mass Spectrom Rev 28:93–120

    Article  PubMed  CAS  Google Scholar 

  • Bai ZF, Liu BY, Li WH, Li P, Wang HL, Wang HX (2009) The development of an improved simple titanium dioxide enrichment method for phosphoproteomic research. Rapid Commun Mass Spectrom 23:3013–3017

    Article  PubMed  CAS  Google Scholar 

  • Beausoleil SA, Jedrychowski M, Schwartz D, Elias JE, Villén J, Li J, Cohn MA, Cantley LC, Gygi SP (2004) Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc Natl Acad Sci U S A 101:12130–12135

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895

    Article  PubMed  CAS  Google Scholar 

  • Bennett J (1979) Chloroplast phosphoproteins. The protein kinase of thylakoid membranes is light-dependent. FEBS Lett 103:342–344

    Article  PubMed  CAS  Google Scholar 

  • Benschop JJ, Mohammed S, O’Flaherty M, Heck AJ, Slijper M, Menke FL (2007) Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol Cell Proteomics 6:1198–1214

    Article  PubMed  CAS  Google Scholar 

  • Bi YD, Wang HX, Lu TC, Li XH, Shen Z, Chen YB, Wang BC (2010) Large-scale analysis of phosphorylated proteins in maize leaf. Planta 233:383–392

    Article  PubMed  Google Scholar 

  • Bodenmiller B, Malmstrom J, Gerrits B, Campbell D, Lam H, Schmidt A, Rinner O, Mueller LN, Shannon PT, Pedrioli PG, Panse C, Lee HK, Schlapbach R, Aebersold R (2007) PhosphoPep—a phosphoproteome resource for systems biology research in Drosophila Kc167 cells. Mol Syst Biol 3:139

    Article  PubMed  PubMed Central  Google Scholar 

  • Boersema PJ, Foong LY, Ding VM, Lemeer S, van Breukelen B, Philp R, Boekhorst J, Snel B, den Hertog J, Choo AB, Heck AJ (2010) In-depth qualitative and quantitative profiling of tyrosine phosphorylation using a combination of phosphopeptide immunoaffinity purification and stable isotope dimethyl labeling. Mol Cell Proteomics 9:84–99

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, Jahns P, Leister D (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437:1179–1182

    Article  PubMed  CAS  Google Scholar 

  • Browning KS, Yan TF, Lauer SJ, Aquino LA, Tao M, Ravel JM (1985) Phosphorylation of wheat germ initiation factors and ribosomal proteins. Plant Physiol 77:370–373

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bunney TD, van Walraven HS, de Boer AH (2001) 14-3-3 protein is a regulator of the mitochondrial and chloroplast ATP synthase. Proc Natl Acad Sci U S A 98:4249–4254

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chi A, Huttenhower C, Geer LY, Coon JJ, Syka JE, Bai DL, Shabanowitz J, Burke DJ, Troyanskaya OG, Hunt DF (2007) Analysis of phosphorylation sites on proteins from Saccharomyces cerevisiae by electron transfer dissociation (ETD) mass spectrometry. Proc Natl Acad Sci U S A 104:2193–2198

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Clarke JB, Britton HG (1974) The mechanism of phosphoglucomutase from Micrococcus lysodeikticus. Biochem J 137:453–461

    PubMed  CAS  PubMed Central  Google Scholar 

  • Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • de la Fuente van Bentem S, Anrather D, Roitinger E, Djamei A, Hufnagl T, Barta A, Csaszar E, Dohnal I, Lecourieux D, Hirt H (2006) Phosphoproteomics reveals extensive in vivo phosphorylation of Arabidopsis proteins involved in RNA metabolism. Nucleic Acids Res 34:3267–3278

    Article  PubMed  CAS  Google Scholar 

  • De Las Rivas J, Roman A (2005) Structure and evolution of the extrinsic proteins that stabilize the oxygen-evolving engine. Photochem Photobiol Sci 4:1003–1010

    Article  Google Scholar 

  • Deng WJ, Nie S, Dai J, Wu JR, Zeng R (2010) Proteome, phosphoproteome, and hydroxyproteome of liver mitochondria in diabetic rats at early pathogenic stages. Mol Cell Proteomics 9:100–116

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Dennis MD, Browning KS (2009) Differential phosphorylation of plant translation initiation factors by Arabidopsis thaliana CK2 holoenzymes. J Biol Chem 284:20602–20614

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Dröge-Laser W, Kaiser A, Lindsay WP, Halkier BA, Loake GJ, Doerner P, Dixon RA, Lamb C (1997) Rapid stimulation of a soybean protein-serine kinase that phosphorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses. EMBO J 16:726–738

    Article  PubMed  PubMed Central  Google Scholar 

  • Elias JE, Gygi SP (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4:207–214

    Article  PubMed  CAS  Google Scholar 

  • Furuya E, Yokoyama M, Uyeda K (1982) Regulation of fructose-6-phosphate 2-kinase by phosphorylation and dephosphorylation: possible mechanism for coordinated control of glycolysis and glycogenolysis. Proc Natl Acad Sci U S A 79:325–329

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gao J, Agrawal GK, Thelen JJ, Xu D (2009) P3DB: a plant protein phosphorylation database. Nucleic Acids Res 37:D960–D962

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gruhler A, Olsen JV, Mohammed S, Mortensen P, Faergeman NJ, Mann M, Jensen ON (2005) Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Mol Cell Proteomics 4:310–327

    Article  PubMed  CAS  Google Scholar 

  • Gu YQ, Yang C, Thara VK, Zhou J, Martin GB (2000) Pti4 is induced by ethylene and salicylic acid, and its product is phosphorylated by the Pto kinase. Plant Cell 12:771–786

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Guo A, He K, Liu D, Bai S, Gu X, Wei L, Luo J (2005) DATF: a database of Arabidopsis transcription factors. Bioinformatics 21:2568–2569

    Article  PubMed  CAS  Google Scholar 

  • Hansson M, Vener AV (2003) Identification of three previously unknown in vivo protein phosphorylation sites in thylakoid membranes of Arabidopsis thaliana. Mol Cell Proteomics 2:550–559

    PubMed  CAS  Google Scholar 

  • Heintz D, Wurtz V, High AA, Van Dorsselaer A, Reski R, Sarnighausen E (2004) An efficient protocol for the identification of protein phosphorylation in a seedless plant, sensitive enough to detect members of signalling cascades. Electrophoresis 25:1149–1159

    Article  PubMed  CAS  Google Scholar 

  • Horton P (1983) Control of chloroplast electron transport by phosphorylation of thylakoid proteins. FEBS Lett 152:47–52

    Article  CAS  Google Scholar 

  • Hunter T (1995) Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80:225–236

    Article  PubMed  CAS  Google Scholar 

  • Hunter T (1998) The Croonian Lecture 1997. The phosphorylation of proteins on tyrosine: its role in cell growth and disease. Philos Trans R Soc Lond B Biol Sci 353:583–605

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hunter T (2000) Signaling-2000 and beyond. Cell 100:113–128

    Article  PubMed  CAS  Google Scholar 

  • Iida K, Seki M, Sakurai T, Satou M, Akiyama K, Toyoda T, Konagaya A, Shinozaki K (2005) RARTF: database and tools for complete sets of Arabidopsis transcription factors. DNA Res 12:247–256

    Article  PubMed  CAS  Google Scholar 

  • Jedrzejas MJ (2000) Structure, function, and evolution of phosphoglycerate mutases: comparison with fructose-2,6-bisphosphatase, acid phosphatase, and alkaline phosphatase. Prog Biophys Mol Biol 73:263–287

    Article  PubMed  CAS  Google Scholar 

  • Kanekatsu M, Saito H, Motohashi K, Hisabori T (1998) The beta subunit of chloroplast ATP synthase (CF0CF1-ATPase) is phosphorylated by casein kinase II. Biochem Mol Biol Int 46:99–105

    PubMed  CAS  Google Scholar 

  • Larsen MR, Thingholm TE, Jensen ON, Roepstorff P, Jørgensen TJ (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol Cell Proteomics 4:873–886

    Article  PubMed  CAS  Google Scholar 

  • Laugesen S, Bergoin A, Rossignol M (2004) Deciphering the plant phosphoproteome: tools and strategies for a challenging task. Plant Physiol Biochem 42:929–936

    Article  PubMed  CAS  Google Scholar 

  • Liu CC, Lu TC, Li HH, Wang HX, Liu GF, Ma L, Yang CP, Wang BC (2010) Phosphoproteomic identification and phylogenetic analysis of ribosomal P-proteins in Populus dormant terminal buds. Planta 231:571–581

    Article  PubMed  CAS  Google Scholar 

  • Ljungberg U, Akerlund HE, Andersson B (1986) Isolation and characterization of the 10-kDa and 22-kDa polypeptides of higher plant photosystem 2. Eur J Biochem 158:477–482

    Article  PubMed  CAS  Google Scholar 

  • Lu TC, Meng LB, Yang CP, Liu GF, Liu GJ, Ma W, Wang BC (2008) A shotgun phosphoproteomics analysis of embryos in germinated maize seeds. Planta 228:1029–1041

    Article  PubMed  CAS  Google Scholar 

  • Lundin B, Hansson M, Schoefs B, Vener AV, Spetea C (2007) The Arabidopsis PsbO2 protein regulates dephosphorylation and turnover of the photosystem II reaction centre D1 protein. Plant J 49:528–539

    Article  PubMed  CAS  Google Scholar 

  • Ma HC, Fung L, Wang SS, Altman A, Hüttermann A (1997) Photosynthetic response of Populus euphratica to salt stress. Forest Ecol Man 93:55–61

    Article  Google Scholar 

  • Macek B, Mijakovic I, Olsen JV, Gnad F, Kumar C, Jensen PR, Mann M (2007) The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol Cell Proteomics 6:697–707

    Article  PubMed  CAS  Google Scholar 

  • Macek B, Gnad F, Soufi B, Kumar C, Olsen JV, Mijakovic I, Mann M (2008) Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol Cell Proteomics 7:299–307

    Article  PubMed  CAS  Google Scholar 

  • Mann M, Jensen ON (2003) Proteomic analysis of post-translational modifications. Nat Biotechnol 21:255–261

    Article  PubMed  CAS  Google Scholar 

  • Mann M, Ong SE, Grønborg M, Steen H, Jensen ON, Pandey A (2002) Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol 20:261–268

    Article  PubMed  CAS  Google Scholar 

  • Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002) The protein kinase complement of the human genome. Science 298:1912–1934

    Article  PubMed  CAS  Google Scholar 

  • Muhlbach H, Schnarrenberger C (1978) Properties and intracellular distribution of two phosphoglucomutases from spinach leaves. Planta 141:65–70

    Article  PubMed  CAS  Google Scholar 

  • Nakagami H, Sugiyama N, Mochida K, Daudi A, Yoshida Y, Toyoda T, Tomita M, Ishihama Y, Shirasu K (2010) Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. Plant Physiol 153:1161–1174

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ning DL, Liu CC, Liu JW, Shen Z, Chen S, Liu F, Wang BC, Yang CP (2013) Label-free quantitative proteomics analysis of dormant terminal buds of poplar. Mol Biol Rep. doi:10.1007/s11033-013-2548-9

    Google Scholar 

  • Nühse TS, Stensballe A, Jensen ON, Peck SC (2004) Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 16:2394–2405

    Article  PubMed  PubMed Central  Google Scholar 

  • Nühse TS, Bottrill AR, Jones AM, Peck SC (2007) Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant J 51:931–940

    Article  PubMed  PubMed Central  Google Scholar 

  • Oda Y, Nagasu T, Chait BT (2001) Enrichment analysis of phosphorylated proteins as a tool for probing the phosphoproteome. Nat Biotechnol 19:379–382

    Article  PubMed  CAS  Google Scholar 

  • Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P, Mann M (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127:635–648

    Article  PubMed  CAS  Google Scholar 

  • Pandey A, Podtelejnikov AV, Blagoev B, Bustelo XR, Mann M, Lodish HF (2000) Analysis of receptor signaling pathways by mass spectrometry: identification of vav-2 as a substrate of the epidermal and platelet-derived growth factor receptors. Proc Natl Acad Sci U S A 97:179–184

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Panichkin VB, Arakawa-Kobayashi S, Kanaseki T, Suzuki I, Los DA, Shestakov SV, Murata N (2006) Serine/threonine protein kinase SpkA in Synechocystis sp. strain PCC 6803 is a regulator of expression of three putative pilA operons, formation of thick pili, and cell motility. J Bacteriol 188:7696–7699

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pawson T, Scott JD (2005) Protein phosphorylation in signaling 50 years and counting. T Trends Biochem Sci 30:286–289

    Article  CAS  Google Scholar 

  • Peri S, Navarro JD, Kristiansen TZ, Amanchy R, Surendranath V, Muthusamy B, Gandhi TK, Chandrika KN, Deshpande N et al (2004) Human protein reference database as a discovery resource for proteomics. Nucleic Acids Res 32:D497–D501

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pinna LA, Ruzzene M (1996) How do protein kinases recognize their substrates? Biochim Biophys Acta 1314:191–225

    Article  PubMed  CAS  Google Scholar 

  • Preisinger C, von Kriegsheim A, Matallanas D, Kolch W (2008) Proteomics and phosphoproteomics for the mapping of cellular signalling networks. Proteomics 8:4402–4415

    Article  PubMed  CAS  Google Scholar 

  • Ptacek J, Devgan G, Michaud G, Zhu H, Zhu X, Fasolo J, Guo H, Jona G, Breitkreutz A, Sopko R, McCartney RR, Schmidt MC, Rachidi N, Lee SJ, Mah AS, Meng L, Stark MJ, Stern DF, De Virgilio C, Tyers M, Andrews B, Gerstein M, Schweitzer B, Predki PF, Snyder M (2005) Global analysis of protein phosphorylation in yeast. Nature 438:679–684

    Article  PubMed  CAS  Google Scholar 

  • Reiland S, Messerli G, Baerenfaller K, Gerrits B, Endler A, Grossmann J, Gruissem W, Baginsky S (2009) Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol 150:889–903

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Riechmann JL (2002) Transcriptional regulation: a genomic overview. The Arabidopsis Book 1–46

  • Rodriguez PL (1998) Protein phosphatase 2C (PP2C) function in higher plants. Plant Mol Biol 38:919–927

    Article  PubMed  CAS  Google Scholar 

  • Salvucci ME, Drake RR, Broadbent KP, Haley BE, Hanson KR, McHale NA (1990) Identification of the 64 kilodalton chloroplast stromal phosphoprotein as phosphoglucomutase. Plant Physiol 93:105–109

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Schmelzle K, White FM (2006) Phosphoproteomic approaches to elucidate cellular signaling networks. Curr Opin Biotechnol 17:406–414

    Article  PubMed  CAS  Google Scholar 

  • Schulze WX (2010) Proteomics approaches to understand protein phosphorylation in pathway modulation. Curr Opin Plant Biol 13:280–287

    Article  PubMed  CAS  Google Scholar 

  • Shen Z, Li P, Ni RJ, Ritchie M, Yang CP, Liu GF, Ma W, Liu GJ, Ma L, Li SJ, Wei ZG, Wang HX, Wang BC (2009) Label-free quantitative proteomics analysis of etiolated maize seedling leaves during greening. Mol Cell Proteomics 8:2443–2460

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sugiyama N, Masuda T, Shinoda K, Nakamura A, Tomita M, Ishihama Y (2007) Phosphopeptide enrichment by aliphatic hydroxy acid-modified metal oxide chromatography for nano-LC-MS/MS in proteomics applications. Mol Cell Proteomics 6:1103–1109

    Article  PubMed  CAS  Google Scholar 

  • Sugiyama N, Nakagami H, Mochida K, Daudi A, Tomita M, Shirasu K, Ishihama Y (2008) Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Mol Syst Biol 4:193–200

    Article  PubMed  PubMed Central  Google Scholar 

  • Suorsa M, Sirpiö S, Allahverdiyeva Y, Paakkarinen V, Mamedov F, Styring S, Aro EM (2006) PsbR, a missing link in the assembly of the oxygen-evolving complex of plant photosystem II. J Biol Chem 281:145–150

    Article  PubMed  CAS  Google Scholar 

  • Tan F, Li G, Chitteti BR, Peng Z (2007) Proteome and phosphoproteome analysis of chromatin associated proteins in rice (Oryza sativa). Proteomics 7:4511–4527

    Article  PubMed  CAS  Google Scholar 

  • Tao WA, Wollscheid B, O’Brien R, Eng JK, Li XJ, Bodenmiller B, Watts JD, Hood L, Aebersold R (2005) Quantitative phosphoproteome analysis using a dendrimer conjugation chemistry and tandem mass spectrometry. Nat Methods 2:591–598

    Article  PubMed  CAS  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Udvardi MK, Kakar K, Wandrey M, Montanari O, Murray J, Andriankaja A, Zhang JY, Benedito V, Hofer JM, Chueng F, Town CD (2007) Legume transcription factors: global regulators of plant development and response to the environment. Plant Physiol 144:538–549

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Villén J, Beausoleil SA, Gerber SA, Gygi SP (2007) Large-scale phosphorylation analysis of mouse liver. Proc Natl Acad Sci U S A 104:1488–1493

    Article  PubMed  PubMed Central  Google Scholar 

  • Vom Endt D, Kijne JW, Memelink J (2002) Transcription factors controlling plant secondary metabolism: what regulates the regulators? Phytochemistry 61:107–114

    Article  PubMed  CAS  Google Scholar 

  • Walker RP, Leegood RC (1996) Phosphorylation of phosphoenolpyruvate carboxykinase in plants. Studies in plants with C4 photosynthesis and Crassulacean acid metabolism and in germinating seeds. Biochem J 317:653–658

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yeung YG, Wang Y, Einstein DB, Lee PS, Stanley ER (1998) Colony-stimulating factor-1 stimulates the formation of multimeric cytosolic complexes of signaling proteins and cytoskeletal components in macrophages. J Biol Chem 273:17128–17137

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Wolf-Yadlin A, Ross PL, Pappin DJ, Rush J, Lauffenburger DA, White FM (2005) Time-resolved mass spectrometry of tyrosine phosphorylation sites in the epidermal growth factor receptor signaling network reveals dynamic modules. Mol Cell Proteomics 4:1240–1250

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful for financial support from the State Key Program of National Natural Science of China (Grant No. 31030017), National Basic Research Priorities Programme (2009CB119102), Fundamental Research Funds for the Central Universities (DL09EA01) and Project of the Natural Sciences Foundation of Heilongjiang Province (Grant C201010) and in part form “The fund for sponsoring the excellent doctor degree dissertation in Northeast Forestry University” (Grap 09).

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Authors and Affiliations

  1. State Key Laboratory of Forest Genetics and Tree Breeding, Northeast Forestry University, 26 Hexing Road, Harbin, 150040, People’s Republic of China

    Jinwen Liu, Deli Ning & Yuxiang Cheng

  2. College of Life Science and Biotechnology, Heilongjiang Bayi Agricultural University, High and New Tech Development Zone, Daqing, 163319, People’s Republic of China

    Jinwen Liu

  3. College of Forestry, Shenyang Agricultural University, Dongling Road 120, Shenyang, Liaoning, 110866, People’s Republic of China

    Guiling Zhao

  4. Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, People’s Republic of China

    Baichen Wang

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  1. Jinwen Liu
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  2. Deli Ning
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  3. Guiling Zhao
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  4. Yuxiang Cheng
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  5. Baichen Wang
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Correspondence to Yuxiang Cheng or Baichen Wang.

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D.-L. Ning and J.-W. Liu contributed equally to this work.

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Liu, J., Ning, D., Zhao, G. et al. Large-scale analysis of protein phosphorylation in Populus leaves. J. Plant Biochem. Biotechnol. 23, 410–420 (2014). https://doi.org/10.1007/s13562-013-0225-7

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