Pre-fractionation strategies to resolve pea (Pisum sativum) sub-proteomes

Frontiers in Plant Science

Volumn 6, Issue October, 2015, Pages

  Meisrimler, Claudia Nicole ^a,b,c,d   Menckhoff, Ljiljana ^a   Kukavica, Biljana M ^e   Lüthje, Sabine ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

^b IRFM   (France)

^c CNRS   (France)

^d University of Aix Marseille   (France)

^e UNIVERSITY OF BANJA LUKA   (Bosnia and Herzegovina)

Author keywords

Apoplast; Cell wall; Chloroplast; Mitochondria; Pisum sativum; Plasma membrane

Indexed keywords

EID: 84947755334     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00849     Document Type: Article

References (60)

1. Alexandersson, E., Ali, A., Resjö, S., and Andreasson, E. (2013). Plant secretome proteomics. Front. Plant. Sci. 4:9. doi: 10.3389/fpls.2013.00009
2. Amey, R. C., Schleicher, T., Slinn, J., Lewis, M., Macdonald, H., Neill, S. J., et al. (2008). Proteomic analysis of a compatible interaction between Pisum sativum (pea) and the downy mildew pathogen Peronospora viciae. Eur. J. Plant Pathol. 122, 41-55. doi: 10.1007/s10658-008-9313-2
3. Aryal, U. K., Krochko, J. E., and Ross, A. R. (2012). Identification of phosphoproteins in Arabidopsis thaliana leaves using polyethylene glycol fractionation, immobilized metal-ion affinity chromatography, two-dimensional gel electrophoresis and mass spectrometry. J. Proteome Res. 11, 425-437. doi: 10.1021/pr200917t
4. 2 during pea seed germination: a combined proteomic and hormone profiling approach. Plant Cell Environ. 34, 1907-1919. doi: 10.1111/j.1365-3040.2011.02386.x
5. Bardel, J., Louwagie, M., Jaquinod, M., Jourdain, A., Luche, S., Rabilloud, T., et al. (2002). A survey of the plant mitochondril proteome in relation to development.Proteomics 2, 880-898. doi: 10.1002/1615-9861(200207)2:7<880::AID-PROT880>3.0.CO;2-0
6. Barilli, E., Rubiales, D., and Castillejo, M. Á. (2012). Comparative proteomic analysis of BTH and BABA-induced resistance in pea (Pisum sativum) toward infection with pea rust (Uromyces pisi). J. Proteomics 75, 5189-5205. doi: 10.1016/j.jprot.2012.06.033
7. Bayer, R. G., Stael, S., Csaszar, E., and Teige, M. (2011). Mining the soluble chloroplast proteome by affinity chromatography. Proteomics 11, 1287-1299. doi: 10.1002/pmic.201000495
8. Beauchamp, C., and Fridovich, I. (1971). Superoxide dismutase: improved assay and assay applicable to acrylamide gels. Anal. Biochem. 44, 276-287. doi: 10.1016/0003-2697(71)90370-8
9. Borner, G. H., Lilley, K. S., Stevens, T. J., and Dupree, P. (2003). Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiol. 132, 568-577. doi: 10.1104/pp.103.021170
10. Bourgeois, M., Jacquin, F., Cassecuelle, F., Savois, V., Belghazi, M., Aubert, G., et al. (2011). A PQL (protein quantity loci) analysis of mature pea seed proteins identifies loci determining seed protein composition. Proteomics 11, 1581-1594. doi: 10.1002/pmic.201000687
11. Bourgeois, M., Jacquin, F., Savois, V., Sommerer, N., Labas, V., Henry, C., et al. (2009). Dissecting the proteome of pea mature seeds reveals the phenotypic plasticity of seed protein composition. Proteomics 9, 254-271. doi: 10.1002/pmic.200700903
12. Bräutigam, A., Hoffmann-Benning, S., and Weber, A. (2008). Comparative proteomics of chloroplast envelopes from C3 and C4 plants reveals specific adaptations of the plastid envelope to C4 photosynthesis and candidate proteins required for maintaining C4 metabolite fluxes. Plant Physiol. 148, 568-579. doi: 10.1104/pp.108.121012
13. Brosowska-Arendt, W., Gallardo, K., Sommerer, N., and Weidner, S. (2014). Changes in the proteome of pea (Pisum sativum L.) seeds germinating under optimal and osmotic stress conditions and subjected to post-stress recovery. Acta Physiol. Plant.36, 795-807. doi: 10.1007/s11738-013-1458-8
14. Castillejo, M. A., Amiour, N., Dumas-Gaudot, E., Rubiales, D., and Jorrín, J. V. (2004). A proteomic approach to study plant response to crenate broomrape (Orobanche crenata) in pea (Pisum sativum). Phytochemistry 65, 1817-1828. doi: 10.1016/j.phytochem.2004.03.029
15. Castillejo, M. Á., Curto, M., Fondevilla, S., Rubiales, D., and Jorrín, J. V. (2010). Two-dimensional electrophoresis based proteomic analysis of the pea (Pisum sativum) in response to Mycoshaerella pinodes. J. Agric. Food Chem. 58, 12822-12832. doi: 10.1021/jf1036917
16. Castillejo, M. Á., Fernández-Aparicio, M., and Rubiales, D. (2011). Proteomic analysis by two-dimensional differential in gel electrophoresis (2D DIGE) of the early response of Pisum sativum to Orobanche crenata. J. Exp. Bot. 63, 107-119. doi: 10.1093/jxb/err246
17. Chen, H., Bodulovic, G., Hall, P. J., Moore, A., Higgins, T. J. V., Djordjevic, M. A., et al. (2009). Unintended changes in protein expression revealed by proteomic analysis of seeds from transgenic pea expressing a bean a-amylase inhibitor gene. Proteomics9, 4406-4415. doi: 10.1002/pmic.200900111
18. Chen, Y., Ye, D., Held, M. A., Cannon, M. C., Ray, T., Saha, P., et al. (2015). Identification of the abundant hydroxyproline-rich glycoproteins in the root walls of wild-type Arabidopsis, an ext3 mutant line, and its phenotypic revertant. Plants 4, 85-111. doi: 10.3390/plants4010085
19. Clemente, A., Carmen Marín-Manzano, M., Jiménez, E., Carmen Arques, M., and Domoney, C. (2012). The anti-proliferative effect of TI1B, a major Bowman-Birk isoinhibitor from pea (Pisum sativum L.), on HT29 colon cancer cells is mediated through protease inhibition. Br. J. Nutr. 108(Suppl. 1), S135-S144 doi: 10.1017/S000711451200075X
20. Curto, M., Camafeita, E., Lopez, J. A., Maldonado, A. M., Rubiales, D., and Jorrín, J. V. (2006). A proteomic approach to study pea (Pisum sativum) responses to powdery mildew (Erysiphe pisi). Proteomics 6, S163-S174. doi: 10.1002/pmic.200500396
21. Dahl, W. J., Foster, L. M., and Tyler, R. T. (2012). Review on the health benefits of peas (Pisum sativum L). Br. J. Nutr. 108(Suppl. 1), S3-S10. doi: 10.1017/S0007114512000852
22. Díaz-Vivancos, P., Clemente-Moreno, M. J., Rubio, M., Olmos, E., García, J. A., Martínez-Gómez, P., et al. (2008). Alterations in the chloroplastic metabolism leads to ROS accumulation in pea plants in response to plum pox virus. J. Exp. Bot. 59, 2147-2160. doi: 10.1093/jxb/ern082
23. Dumont, E., Bahrman, N., Goulas, E., Valot, B., Sellier, H., Hilbert, J. L., et al. (2011). A proteomic approach to decipher chilling response from cold acclimation in pea (Pisum sativum L.). Plant Sci. 180, 86-98. doi: 10.1016/j.plantsci.2010.09.006
24. Dziuba, J., Szerszunowicz, I., Nałęz, D., and Dziuba, M. (2014). Proteomic analysis of albumin and globulin fractions of pea (Pisum sativum L.) seeds. Acta Sci. Pol. Technol. Aliment. 13, 181-190. doi: 10.17306/J.AFS.2014.2.7
25. Franssen, S. U., Shrestha, R. P., Bräutigam, A., Bornberg-Bauer, E., and Weber, A. P. (2011). Comprehensive transcriptome analysis of the highly complex Pisum sativumgenome using next generation sequencing. BMC Genomics 12:227. doi: 10.1186/1471-2164-12-227
26. Giavalisco, P., Nordhoff, E., Lehrach, H., Gobom, J., and Klose, J. (2003). Extraction of proteins from plant tissues for two-dimensional electrophoresis analysis.Electrophoresis 24, 207-216. doi: 10.1002/elps.200390016
27. Gómez, S. M., Nishio, J. N., Faull, K. F., and Whitelegge, J. P. (2002). The chloroplast grana proteome defined by intact mass measurements from liquid chromatography mass spectrometry. Mol. Cell. Proteomics 1, 46-59. doi: 10.1074/mcp.M100007-MCP200
28. Grant, J., and Cooper, P. (2006). Peas (Pisum sativum L.). Methods Mol. Biol. 343, 337-346. doi: 10.1385/1-59745-130-4:337
29. Gutierrez-Carbonell, E., Takahashi, D., Lattanzio, G., Rodríguez-Celma, J., Kehr, J., Soll, J., et al. (2014). The distinct functional roles of the inner and outer chloroplast envelope of Pea (Pisum sativum) as revealed by proteomic approaches. J. Proteome Res. 13, 2941-2953. doi: 10.1021/pr500106s
30. 3+-Chelate reductase activity of plasma membranes isolated from tomato (Lycopersicon esculentum Mill.) roots. Plant Physiol. 97, 537-544. doi: 10.1104/pp.97.2.537
31. Jamet, E., Canut, H., Boudart, G., and Pont-Lezica, R. F. (2006). Cell wall proteins: a new insight through proteomics. Trends Plant. Sci. 11, 33-39. doi: 10.1016/j.tplants.2005.11.006
32. Kaló, P., Seres, A., Taylor, S. A., Jakab, J., Kevei, Z., Kereszt, A., et al. (2004). Comparative mapping between Medicago sativa and Pisum sativum. Mol. Gen. Genomics 272, 235-246. doi: 10.1007/s00438-004-1055-z
33. Kanervo, E., Singh, M., Suorsa, M., Paakkarinen, V., Aro, E., Battchikova, N., et al. (2008). Expression of protein complexes and individual proteins upon transition of etioplasts to chloroplasts in pea (Pisum sativum). Plant Cell Physiol. 49, 396-410. doi: 10.1093/pcp/pcn016
34. Kav, N. N. V., Srivastava, S., Goonewardene, L., and Blade, S. F. (2004). Proteome-level changes in the roots of Pisum sativum in response to salinity. Ann. Appl. Biol.145, 217-230. doi: 10.1111/j.1744-7348.2004.tb00378.x
35. Kinoshita, E., and Kinoshita-Kikuta, E. (2011). Improved Phos-tag SDS-PAGE under neutral pH conditions for advanced protein phosphorylation profiling. Proteomics 11, 319-323. doi: 10.1002/pmic.201000472
36. Krishnan, H. B., and Natarajan, S. S. (2009). A rapid method for depletion of Rubisco from soybean (Glycine max) leaf for proteomic analysis of lower abundance proteins.Phytochemistry 70, 1958-1964. doi: 10.1016/j.phytochem.2009.08.020
37. Kukavica, B. M., Veljovicć-Jovanovicć, S. D., Menckhoff, L., and Lüthje, S. (2012). Cell wall-bound cationic and anionic class III isoperoxidases of pea root: biochemical characterization and function in root growth. J. Exp. Bot. 63, 4631-4645. doi: 10.1093/jxb/ers139
38. Ladig, R., Sommer, M. S., Hahn, A., Leisegang, M. S., Papasotiriou, D. G., Ibrahim, M., et al. (2011). A high-definition native polyacrylamide gel electrophoresis system for the analysis of membrane complexes. Plant J. 67, 181-194. doi: 10.1111/j.1365-313X.2011.04577.x
39. Lüthje, S., Meisrimler, C. N., Hopff, D., Schütze, T., Köppe, J., and Heino, K. (2014). "Class III peroxidases," in Methods in Molecular Plant Biology, Plant Proteomics: Methods and Protocols, 2nd Edn, eds Jorrín Novo, J. V., Komatsu, S., Weckwerth, W., Wienkoop, S. (New York, NY: Humana Press Inc.), 687-706.
40. Macas, J., Neumann, P., and Navrátilová, A. (2007). Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics 8:427. doi: 10.1186/1471-2164-8-427
41. Meisrimler, C.-N., and Lüthje, S. (2012). IPG-strips versus off-gel fractionation: advantages and limits of two-dimensional PAGE in separation of microsomal fractions of frequently used plant species and tissues. J. Proteomics 75, 2550-2562. doi: 10.1016/j.jprot.2012.02.026
42. Meisrimler, C.-N., Planchon, S., Renaut, J., Sergeant, K., and Lüthje, S. (2011). Alteration of plasma membrane-bound redox systems of iron deficient pea root by chitosan. J. Proteomics 4, 1437-1449. doi: 10.1016/j.jprot.2011.01.012
43. Meisrimler, C.-N., Schwendke, A., and Lüthje, S. (2015). Two-dimensional phos-tag zymograms for tracing phosphoproteins by activity in-gel staining. Front. Plant Sci.6:230. doi: 10.3389/fpls.2015.00230
44. Mika, A., Boenisch, M. J., Hopff, D., and Lüthje, S. (2010). Membrane-bound guaiacol peroxidases are regulated by methyl jasmonate, salicylic acid, and pathogen elicitors.J. Exp. Bot. 61, 831-841. doi: 10.1093/jxb/erp353
45. Minic, Z., Rihouey, C., Do, C. T., Lerouge, P., and Jouanin, L. (2004). Purification and characterization of enzymes exhibiting β-D-xylosidase activities in stem tissues of Arabidopsis. Plant Physiol. 135, 867-878. doi: 10.1104/pp.104.041269
46. Mustafa, G., and Komatsu, S. (2014). Quantitative proteomics reveals the effect of protein glycosylation in soybean root under flooding stress. Front. Plant Sci. 5:627. doi: 10.3389/fpls.2014.00627
47. Pagliano, C., Nield, J., Marsano, F., Pape, T., Barera, S., Saracco, G., et al. (2014). Proteomic characterization and three-dimensional electron microscopy study of PSII-LHCII supercomplexes from higher plants. Biochim. Biophys. Acta 1837. 1454-1462. doi: 10.1016/j.bbabio.2013.11.004
48. Phinney, B. S., and Thelen, J. J. (2005). Proteomic characterization of a triton-insoluble fraction from chloroplast defines a novel group of proteins associated with macromolecular structures. J. Proteome Res. 4, 497-506. doi: 10.1021/pr049791k
49. Rothe, G. M. (1994). Electrophoresis of Enzymes. Berlin: Springer Verlag.
50. Saalbach, G., Erik, P., and Wienkoop, S. (2002). Characterization by proteomics of peribacteroid space and peribacteroid membrane preparations from pea (Pisum sativum) symbiosomes. Proteomics 2, 325-337. doi: 10.1002/1615-9861(200203)2:3<325::AID-PROT325>3.0.CO;2-W
51. Schiltz, S., Gallardo, K., Huart, M., Negroni, L., Sommerer, N., and Burstin, J. (2004). Proteome reference maps of vegetative tissues in pea. An investigation of nitrogen mobilization from leaves during seed filling. Plant Physiol. 135, 2241-2260. doi: 10.1104/pp.104.041947
52. Singh, R., Chénier, D., Bériault, R., Mailloux, R., Hamel, R. D., and Appanna, V. D. (2005). Blue native polyacrylamide gel electrophoresis and the monitoring of malate- and oxaloacetate-producing enzymes. J. Biochem. Biophys. Meth. 64, 189-199. doi: 10.1016/j.jbbm.2005.07.005
53. Smith-Hammond, C. L., Hoyos, E., and Miernyk, J. A. (2014). The pea seedling mitochondrial Nε-lysine acetylome. Mitochondrion 19, 154-165. doi: 10.1016/j.mito.2014.04.012
54. Tarchevsky, I. A., Yakovleva, V. G., and Egorova, A. M. (2010). Proteomic analysis of salicylate-induced proteins of pea (Pisum sativum L.) leaves. Biochem. (Moscow) 75, 590-597. doi: 10.1134/S0006297910050081
55. Taylor, N. L., Heazlewood, J. L., Day, D. A., and Millar, A. H. (2005). Differential impact of environmental stresses on the pea mitochondrial proteome. Mol. Cell Proteomics 4, 1122-1133. doi: 10.1074/mcp.M400210-MCP200
56. Wang, H., Chang-Wong, T., Tang, H. Y., and Speicher, D. W. (2010). Comparison of extensive protein fractionation and repetitive LC-MS/MS analyses on depth of analysis for complex proteomes. J. Proteome Res. 9, 1032-1040. doi: 10.1021/pr900927y
57. Wang, W. Q., Møller, I. M., and Song, S. Q. (2012). Proteomic analysis of embryonic axis of Pisum sativum seeds during germination and identification of proteins associated with loss of desiccation tolerance. J. Proteomics 77, 68-86. doi: 10.1016/j.jprot.2012.07.005
58. Witzel, K., Shahzad, M., Matros, A., Mock, H. P., and Mühling, K. H. (2011). Comparative evaluation of extraction methods for apoplastic proteins from maize leaves. Plant Methods 7:48. doi: 10.1186/1746-4811-7-48
59. Wu, X., Xiong, E., Wang, W., Scali, M., and Cresti, M. (2014). Universal sample preparation method integrating trichloroacetic acid/acetone precipitation with phenol extraction for crop proteomic analysis. Nat. Protoc. 9, 362-374. doi: 10.1038/nprot.2014.022
60. Zhou, L. Bokhari, S. A., Dong, C. J., and Liu, J. Y. (2011). Comparative proteomics analysis of the root apoplasts of rice seedlings in response to hydrogen peroxide. PLoS ONE. 6:e16723. doi: 10.1371/journal.pone.0016723