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A systemic proteomic analysis of Populus chloroplast by using shotgun method

Molecular Biology Reports volume 38, pages 3045–3054 (2011)Cite this article

Abstract

The chloroplast is one of the most important organelles in plants. Proteomic investigations of chloroplasts have been undertaken for many herb plant species, but to date no such investigation has been reported for woody plant chloroplasts. In the present study we initiated a systematic proteomic study of Populus chloroplasts using a shotgun proteomic method. After isolation of chloroplasts and tryptic digestion of the proteins, the protein fragments were separated via HPLC using an SCX column, and the peptides were analyzed by LC-MS/MS; 119 proteins were successfully identified. Based on annotation information in the UniProtKB/Swiss-Prot database, these proteins were identified as being localized in the chloroplast thylakoid membrane, chloroplast stroma, chloroplast thylakoid lumen, and plastoglobules. Over 50% of all identified proteins were confirmed as chloroplast thylakoid proteins, and 85 are encoded by the chloroplast genome with the remaining proteins encoded by the nuclear genome. Based on functional annotation, these proteins were classified into four functional categories, including photosynthesis, redox regulation and stress, primary and secondary metabolism, transport and signaling. These data provide a valuable basis for further studies on photosynthesis in poplar species.

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References

  1. Plomion C, Lalanne C, Claverol S et al (2006) Mapping the proteome of poplar and application to the discovery of drought-stress responsive proteins. Proteomics 6:6509–6527

    PubMed  Article  CAS  Google Scholar 

  2. Yin TM, DiFazio SP, Gunter LE et al (2004) Large-scale heterospecific segregation distortion in Populus revealed by a dense genetic map. Theor Appl Genet 109:451–463

    PubMed  Article  CAS  Google Scholar 

  3. Zhang D, Zhang Z, Yang K et al (2004) Genetic mapping in (Populus tomentosa xPopulus bolleana) and P.tomentosa Carr. Using AFLP markers. Theor Appl Genet 108:657–662

    PubMed  Article  CAS  Google Scholar 

  4. Cervera MT, Storme V, Soto A et al (2005) Intraspecific and interspecific genetic and phylogenetic relationships in the genus Populus based on AFLP markers. Theor Appl Genet 111:1440–1456

    PubMed  Article  CAS  Google Scholar 

  5. Woolbright SA, DiFazio SP, Yin T et al (2008) A dense linkage map of hybrid cottonwood (Populus fremontii x P. angustifolia) contributes to long-term ecological research and comparison mapping in a model forest tree. Heredity 100:59–70

    PubMed  Article  CAS  Google Scholar 

  6. Kelleher CT, Chiu R, Shin H et al (2007) A physical map of the highly heterozygous Populus genome: integration with the genome sequence and genetic map and analysis of haplotype variation. Plant J 50:1063–1078

    PubMed  Article  CAS  Google Scholar 

  7. Andersson A, Keskitalo J, Sjodin A et al (2004) A transcriptional timetable of autumn senescence. Genome Biol 5:R24

    PubMed  Article  Google Scholar 

  8. Brosche M, Vinocur B, Alatalo ER et al (2005) Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert. Genome Biol 6:R101

    PubMed  Article  Google Scholar 

  9. Harding SA, Jiang H, Jeong ML et al (2005) Functional genomics analysis of foliar condensed tannin and phenolic glycoside regulation in natural cottonwood hybrids. Tree Physiol 25:1475–1486

    PubMed  CAS  Google Scholar 

  10. Ralph S, Oddy C, Cooper D et al (2006) Genomics of hybrid poplar (Populus trichocarpa x deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Mol Ecol 15:1275–1297

    PubMed  Article  Google Scholar 

  11. Bhalerao R, Keskitalo J, Sterky F et al (2003) Gene expression in autumn leaves. Plant Physiol 131:430–442

    PubMed  Article  Google Scholar 

  12. Kohler A, Delaruelle C, Martin D et al (2003) The poplar root transcriptome: analysis of 7000 expressed sequence tags. FEBS Lett 542:37–41

    PubMed  Article  Google Scholar 

  13. Schrader J, Moyle R, Bhalerao R et al (2004) Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J 40:173–187

    PubMed  Article  CAS  Google Scholar 

  14. Sterky F, Bhalerao RR, Unneberg P et al (2004) A Populus EST resource for plant functional genomics. Proc Natl Acad Sci USA 101:13951–13956

    PubMed  Article  Google Scholar 

  15. Christopher ME, Miranda M, Major IT et al (2004) Gene expression profiling of systemically wound-induced defenses in hybrid poplar. Planta 219:936–947

    PubMed  Article  CAS  Google Scholar 

  16. Nanjo T, Futamura N, Nishiguchi M et al (2004) Characterization of full-length enriched expressed sequence tags of stress-treated poplar leaves. Plant Cell Physiol 45:1738–1748

    PubMed  Article  Google Scholar 

  17. Rishi AS, Munir S, Kapur V et al (2004) Identification and analysis of safener-inducible expressed sequence tags in Populus using acDNA microarray. Planta 220:296–306

    PubMed  Article  CAS  Google Scholar 

  18. Baginsky S, Gruissem W (2004) Chloroplast proteomics: potentials and challenges. J Exp Bot 55:1213–1220

    PubMed  Article  CAS  Google Scholar 

  19. Kislinger T, Emili A (2003) Going global: protein expression profiling using shotgun mass spectrometry. Curr Opin Mol Ther 5:285–293

    PubMed  CAS  Google Scholar 

  20. Yates JR, Eng JK, McCormack AL et al (1995) Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal Chem 67:1426–1436

    PubMed  Article  CAS  Google Scholar 

  21. Perkins DN, Pappin DJ, Creasy DM et al (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551–3567

    PubMed  Article  CAS  Google Scholar 

  22. Taylor SW, Fahy E, Ghosh SS et al (2003) Global organellar proteomics. Trends Biotechnol 21:82–88

    PubMed  Article  CAS  Google Scholar 

  23. Peltier JB, Cai Y, Sun Q et al (2006) The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol Cell Proteomics 5:114–133

    PubMed  CAS  Google Scholar 

  24. Monde RA, Schuster G, Stern DB (2000) Processing and degradation of chloroplast mRNA. Biochimie 82:573–582

    PubMed  Article  CAS  Google Scholar 

  25. Barkan A, Goldschmidt-Clermont M (2000) Participation of nuclear genes in chloroplast gene expression. Biochimie 82:559–572

    PubMed  Article  CAS  Google Scholar 

  26. Gallardo K, Job C, Groot SP et al (2002) Proteomics of Arabidopsis seed germination. A comparative study of wild-type and gibberellin-deficient seeds. Plant Physiol 129:823–837

    PubMed  Article  CAS  Google Scholar 

  27. Brugière S, Kowalski S, Ferro M et al (2004) The hydrophobic proteome of mitochondrial membranes from Arabidopsis cell suspensions. Phytochemistry 65:1693–1707

    PubMed  Article  Google Scholar 

  28. Ferro M, Salvi D, Brugière S et al (2003) Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol Cell Proteomics 2:325–345

    PubMed  CAS  Google Scholar 

  29. Giavalisco P, Nordhoff E, Kreitler T et al (2005) Proteome analysis of Arabidopsis thaliana by two-dimensional gel electrophoresis and matrix-assisted laser desorption/ionisation-time of flight mass spectrometry. Proteomics 5:1902–1913

    PubMed  Article  CAS  Google Scholar 

  30. Rakwal R, Agrawal GK (2003) Rice proteomics: current status and future perspectives. Electrophoresis 24:3378–3389

    PubMed  Article  CAS  Google Scholar 

  31. Watson BS, Asirvatham VS, Wang L et al (2003) Mapping the proteome of barrel medic(Medicago truncatula). Plant Physiol 131:1104–1123

    PubMed  Article  Google Scholar 

  32. Mathesius U, Keijzers G, Natera SH et al (2001) Establishment of a root proteome reference map for the model legume Medicago truncatula using the expressed sequence tag database for peptide mass fingerprinting. Proteomics 1:1424–1440

    PubMed  Article  CAS  Google Scholar 

  33. Lei Z, Elmer AM, Watson BS et al (2005) A two-dimensional electrophoresis proteomic reference map and systematic identification of 1367 proteins from a cell suspension culture of the model legume Medicago truncatula. Mol Cell Proteomics 4:1812–1825

    PubMed  Article  CAS  Google Scholar 

  34. Donnelly BE, Madden RD, Ayoubi P et al (2005) The wheat (Triticum aestivum L.) leaf proteome. Proteomics 5:1624–1633

    PubMed  Article  CAS  Google Scholar 

  35. Bahrman N, Le Gouis J, Negroni L et al (2004) Differential protein expression assessed by two-dimensional gel electrophoresis for two wheat varieties grown at four nitrogen levels. Proteomics 4:709–719

    PubMed  Article  CAS  Google Scholar 

  36. Hanaphthy A, Stein JW, Thelen JJ (2005) A systematic proteomic study of seed filling in soybean. Establishment of high-resolution two-dimensional reference maps, expression profiles, and an interactive proteome database. Plant Physiol 137:1397–1419

    Article  Google Scholar 

  37. Schiltz S, Gallardo K, Huart M et al (2004) Proteome reference maps of vegetative tissues in pea. An investigation of nitrogen mobilization from leaves during seed filling. Plant Physiol 135:2241–2260

    PubMed  Article  CAS  Google Scholar 

  38. Méchin V, Balliau T, Château-Joubert S et al (2004) A two-dimensional proteome map of maize endosperm. Phytochemistry 65:1609–1618

    PubMed  Article  Google Scholar 

  39. Costa P, Pionneau C, Bauw G et al (1999) Separation and characterization of needle and xylem maritime pine proteins. Electrophoresis 20:1098–1108

    PubMed  Article  CAS  Google Scholar 

  40. Gion JM, Lalanne C, Le Provost G et al (2005) The proteome of maritime pine wood forming tissue. Proteomics 5:3731–3751

    PubMed  Article  CAS  Google Scholar 

  41. Jorge I, Navarro RM, Lenz C et al (2005) The holm oak leaf proteome: analytical and biological variability in the protein expression level assessed by 2-DE and protein identification tandem mass spectrometry de novo sequencing and sequence similarity searching. Proteomics 5:222–234

    Google Scholar 

  42. Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa. Science 313:1596–1604

    PubMed  Article  CAS  Google Scholar 

  43. Ni RJ, Shen Z, Yang CP et al (2010) Identification of low abundance polyA-binding proteins in Arabidopsis chloroplast using polyA-affinity column. Mol Biol Rep 37:637–641

    PubMed  Article  CAS  Google Scholar 

  44. Lu TC, Meng LB, Yang CP et al (2008) A shotgun phosphoproteomics analysis of embryos in germinated maize seeds. Planta 228:1029–1041

    PubMed  Article  CAS  Google Scholar 

  45. Friso G, Giacomelli L (2004) In-depth analysis of the thylakoid membrane proteome of arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. Plant Cell 16:478–499

    PubMed  Article  CAS  Google Scholar 

  46. van Wijk KJ (2000) Proteomics of the chloroplast experimentation and prediction. Trends Plant Sci 5:420–425

    Google Scholar 

  47. Schlicher T, Soll J (1996) Molecular chaperones are present in the thylakoid lumen of pea chloroplasts. FEBS Lett 379:302–304

    PubMed  Article  CAS  Google Scholar 

  48. Fulgosi H, Vener AV, Altschmied L et al (1998) A novel multi-functinal chloroplast proteins: identification of a 40 kDa immunophilin-like protein located in the thylakoid lumen. EMBO J 17:1577–1587

    PubMed  Article  CAS  Google Scholar 

  49. Park YI, Karlsson J, Rojdestvenski I et al (1999) Role of a novel photosystem II-associated carbonic anhydrase in photosynthetic carbon assimilation in Chlamydomonas reinhardtii. FEBS Lett 444:102–105

    PubMed  Article  CAS  Google Scholar 

  50. Hieber AD, Bugos RC, Yamamoto HY et al (2000) Plant lipocalins: violaxanthin de-epoxidase and zeaxanthin epoxidase. Biochim Biophys Acta 1482:84–91

    PubMed  Article  CAS  Google Scholar 

  51. Kiedelbach T, Bystedt M, Hynds P et al (2000) A peroxidase homologue and novel plastocyanin located by proteomics to the Arabidopsis chloroplast thylakoid lumen. FEBS Lett 480:271–276

    Article  Google Scholar 

  52. Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol 118:9–17

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

Financial support was obtained from the National Natural Sciences Foundation of China (grant number 30571513) and the Basic Natural Sciences Foundation of Northeast Forestry University (grant number 010-602049).

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Affiliations

  1. Key Laboratory of Forest Tree Genetic Improvement and Biotechnology, Ministry of Education, Northeast Forestry University, 26 Hexing Road, Harbin, 150040, China

    Hong-Mei Yuan, Kai-Long Li, Rui-Juan Ni, Zhuo Shen, Chuan-Ping Yang, Bai-Chen Wang, Gui-Feng Liu & Jing Jiang

  2. College of Life Science, Daqing Normal University, Xibinxi Road, Daqing, 163712, China

    Hong-Mei Yuan

  3. Institute of Natural Resources and Ecology, Heilongjiang Academy of Sciences, 103 Haping Road, Harbin, 150040, China

    Wen-Dong Guo

  4. College of Life Science and Biotechnology, Harbin Normal University, 50 Hexing Road, Harbin, 150080, China

    Chang-Hong Guo

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  1. Hong-Mei Yuan
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  2. Kai-Long Li
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  9. Chang-Hong Guo
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  10. Jing Jiang
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Corresponding author

Correspondence to Jing Jiang.

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Hong-Mei Yuan, Kai-Long Li contributed equally to the work.

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Yuan, HM., Li, KL., Ni, RJ. et al. A systemic proteomic analysis of Populus chloroplast by using shotgun method. Mol Biol Rep 38, 3045–3054 (2011). https://doi.org/10.1007/s11033-010-9971-y

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  • DOI: https://doi.org/10.1007/s11033-010-9971-y

Keywords

  • Populus chloroplast
  • Shotgun
  • SCX
  • Proteomics