The analysis of Lupinus albus root proteome revealed cytoskeleton altered features due to long-term boron deficiency

Journal of Proteomics

Volumn 74, Issue 8, 2011, Pages 1351-1363

  Alves, M ^a   Moes, S ^b   Jeno P ^b   Pinheiro, C ^a   Passarinho, J ^c   Ricardo, C P ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b UNIVERSITY OF BASEL   (Switzerland)

^c Instituto Nacional de Recursos Biológicos L INIA   (Portugal)

Author keywords

Boron deficiency; Cytoskeleton; Lupinus albus; Proteomics; Root

Indexed keywords

BORON; ISOPROTEIN; POLYPEPTIDE; PROTEOME;

AMINO ACID METABOLISM; ARTICLE; BIOSYNTHESIS; CELL METABOLISM; CELL WALL; CYTOSKELETON; ENERGY METABOLISM; LUPINUS ALBUS; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT GROWTH; PLANT MORPHOLOGY; PLANT ROOT; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN MODIFICATION; TWO DIMENSIONAL ELECTROPHORESIS;

BORON; CYTOSKELETAL PROTEINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION PROFILING; LUPINUS; PLANT PROTEINS; PLANT ROOTS; PROTEOME;

LUPINUS ALBUS;

EID: 79960993102     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.03.002     Document Type: Article

References (69)

1. Warington K. The effect of boric acid and borax on the broad bean and certain other plants. Ann Bot 1923, 37:629-672.
2. Nable R., Bañuelos G., Paul J. Boron toxicity. Plant Soil 1997, 193:181-198.
3. Shorrocks V.M. The occurrence and correction of boron deficiency. Plant Soil 1997, 193:121-148.
4. Vale R.R. Efeito da deficiência de boron na produção de matéria seca e semente de trevo subterrâneo. Pastagens Forragens 1995, 16:9-19.
5. Cakmak I., Römheld V. Boron deficiency-induced impairments of cellular functions in plants. Plant Soil 1997, 193:71-83.
6. Brown P., Bellaloui N., Wimmer M., Bassil E., Ruiz J., Hu H., et al. Boron in plant biology. Plant Biol 2002, 4:203-223.
7. Kobayashi M., Matoh T., Azuma J. Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higher plant cell walls. Plant Physiol 1996, 110:1017-1020.
8. O'Neill M., Warrenfeltz D., Kates K., Pellerin P., Doco T., Darvill A., et al. Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cell, forms a dimer that is covalently cross linked by a borate ester. J Biol Chem 1996, 271:22923-22930.
9. O'Neill M., Eberhard S., Albersheim P., Darvill A. Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 2001, 294:846-849.
10. Nielsen F. Boron in human and animal nutrition. Plant Soil 1997, 193:199-208.
11. Park M., Li Q., Shecheynikov N., Muallem S., Zeng W. Borate transport and cell growth and proliferation: not only in plants. Cell Cycle 2005, 4:24-26.
12. Unver T., Bozkurt O., Akkaya M.S. Identification of differentially expressed transcripts from leaves of the boron tolerant plant Gypsophila perfoliata L. Plant Cell Rep 2008, 27:1411-1422.
13. Zeng C., Han Y., Shi L., Peng L., Wang Y., Xu F., et al. Genetic analysis of the physiological responses to low boron stress in Arabidopsis thaliana. Plant Cell Environ 2008, 31:112-122.
14. Koshiba T., Kobayashi M., Matoh T. Boron nutrition of tobacco BY-2 cells. V. Oxidative damage is the major cause of cell death induced by boron deprivation. Plant Cell Physiol 2009, 50:26-36.
15. Kasajima I., Ide Y., Hirai M.Y., Fujiwara T. WRKY6 is involved in the response to boron deficiency in Arabidopsis thaliana. Physiol Plant 2010, 139:80-92.
16. Patterson J., Ford K., Cassin A., Natera S., Bacic A. Increased abundance of proteins involved in phytosiderophore production in boron-tolerant barley. Plant Physiol 2007, 144:1612-1631.
17. Ahsan N., Renaut J., Komatsu S. Recent developments in the application of proteomics to the analysis of plant responses to heavy metals. Proteomics 2009, 9:2602-2621.
18. Wang Z., Wang Z., Shi L., Wang L., Xu F. Proteomic alterations of Brassica napus root in response to boron deficiency. Plant Mol Biol 2010, 74:265-278.
19. Alves M., Francisco R., Martins I., Ricardo C. Proteomic analysis of the extracellular domain of Lupinus albus leaves in response to boron deficiency. Plant Soil 2006, 279:1-11.
20. Alves M, Chicau P, Matias H, Passarinho J, Pinheiro C, Ricardo CP (in press) Metabolic analysis revealed altered amino acid profiles in Lupinus albus organs due to boron deficiency. Physiol Plant.
21. Lupins as crop plants: biology, production and utilization 1998, CAB International, Wallingford, UK. J.S. Gladstones, C.A. Atkins, J. Hamblin (Eds.).
22. Fitter A. Characteristics and functions of root systems. Plant roots: the hidden half 2002, 3-25. CRC Press, New York. Y. Waisel, A. Eshel, U. Kafkafi (Eds.).
23. Arnon D. Microelements in culture-solution experiment with higher plants. Am J Bot 1938, 25:322-325.
24. Ramagli L. Quantifying protein in 2D PAGE solubilization buffers. Methods in molecular biology - 2D proteome analysis protocols 1999, 95-105. Humana Press, Totowa, NJ. A.J. Link (Ed.).
25. Laemmli U. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
26. Neuhoff V., Stamm R., Eibl H. Clear background and highly sensitive protein staining with Coomassie Blue dyes in polyacrylamide gels: a systematic analysis. Electrophoresis 1985, 6:427-448.
27. Quackenbush J. Microarray data normalization and transformation. Nat Genet 2002, 32:496-501.
28. Meunier B., Bouley J., Piec I., Bernard C., Picard B., Hocquette J.-F. Data analysis methods for detection of differential protein expression in two-dimensional gel electrophoresis. Anal Biochem 2005, 340:226-230.
29. Gatlin C., Eng J., Cross S., Detter J., Yates J. Automated identification of amino acid sequence variations in proteins by HPLC/microspray tandem mass spectrometry. Anal Chem 2000, 72:757-763.
30. Thioulouse J., Dray S. Interactive multivariate data analysis in R with the ade4 and ade4TkGUI packages. J Stat Softw 2007, 22:1-14.
31. Lim H., Eng J., Yates J.R., Tollaksen S.L., Giometti C.S., Holden J.F., et al. Identification of 2D-gel proteins: a comparison of MALDI/TOF peptide mass mapping to μ LC-ESI tandem mass spectrometry. J Am Soc Mass Spectrom 2003, 14:957-970.
32. Stitt M. Pyrophosphate as an alternative energy donor in the cytosol of plant cells: an enigmatic alternative to ATP. Bot Acta 1998, 111:167-175.
33. Ferrol N., Donaire J. Effect of boron on plasma membrane proton extrusion and redox activity in sunflower cells. Plant Sci 1992, 86:41-47.
34. Luethy M., Gemel J., Johnston M., Mooney B., Miernyk J., Randall D. Developmental expression of the mitochondrial pyruvate dehydrogenase complex in pea (Pisum sativum) seedlings. Physiol Plant 2001, 112:559-566.
35. Tovar-Méndez A., Miernyk J., Randall D. Regulation of pyruvate dehydrogenase complex activity in plant cells. FEBS J 2003, 270:1043-1049.
36. Moeder W., Pozo O., Navarre D., Martin G., Klessig D. Aconitase plays a role in regulating resistance to oxidative stress and cell death in Arabidopsis and Nicotiana benthamiana. Plant Mol Biol 2007, 63:273-287.
37. Timperio A., Giulia M., Zolla L. Proteomics applied on plant abiotic stress: role of heat shock proteins (HSP). J Proteomics 2008, 71:391-411.
38. Nuc K., Nuc P., Slomski R. Yellow lupine cyclophilin transcripts are highly accumulated in the nodule meristem zone. Mol Plant-Microbe Interact 2001, 14:1384-1394.
39. Rospert S., Dubaquie Y., Gautschi M. Nascent-polypeptide associated complex. Cell Mol Life Sci 2002, 59:1632-1639.
40. Voigt G., Biehl B., Heinrichs H., Voigt J. Aspartic proteinase levels in seeds of different angiosperms. Phytochemistry 1997, 44:389-392.
41. Hochachka P., Lutz P. Mechanism, origin and evolution of anoxia tolerance in animals. Comp Biochem Physiol 2001, 130:435-459.
42. Han S., Chen L., Jiang H., Smith B., Yang L., Xie C. Boron deficiency decreases growth and photosynthesis, and increases starch and hexoses in leaves of citrus seedlings. J Plant Physiol 2008, 165:1331-1341.
43. Kobayashi M., Mutoh T., Matoh T. Boron nutrition of cultured tobacco BY-2 cells. IV. Genes induced under low boron supply. J Exp Bot 2004, 55:1441-1443.
44. Martinoia E., Rentsch D. Malate compartmentation-responses to a complex metabolism. Annu Rev Plant Physiol Plant Mol Biol 1994, 45:447-467.
45. Higuchi T. Lignin biochemistry: biosynthesis and biodegradation. Wood Sci Technol 1990, 24:23-63.
46. Blevins D., Lukaszewski K. Boron in plant structure and function. Annu Rev Plant Physiol Plant Mol Biol 1998, 49:481-500.
47. Dell B., Malajczuk N. Boron deficiency in eucalypt plantations in China. Can J Res 1994, 24:2409-2416.
48. Watanabe A., Nong V., Zhang D., Arahira M., Yeboah N., Udaka K., et al. Molecular cloning and ethylene-inducible expression of Chib1 chitinase from soybean. Biosci Biotechnol Biochem 1999, 63:251-256.
49. Van Loon L., Van Strien E. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 1999, 55:85-97.
50. Kvint K., Nachin L., Diez A., Nyström T. The bacterial universal stress protein: function and regulation. Curr Opin Microbiol 2003, 6:140-145.
51. Bernier F., Berna A. Germins and germin-like proteins: plant do-all proteins. But what do they do exactly?. Plant Physiol Biochem 2001, 39:545-554.
52. Reguera M., Bonilla I., Bolaños L. Boron deficiency results in induction of pathogenesis-related proteins from the PR-10 family during the legume-rhizobia interaction. J Plant Physiol 2010, 167:625-632.
53. Kasprzewska A. Plant chitinases - regulation and function. Cell Mol Biol Lett 2003, 8:809-824.
54. Liu J.-J., Ekramoddoullah A. The family 10 of plant pathogenesis-related proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiol Mol Plant Pathol 2006, 68:3-13.
55. Haizel T., Merkle T., Pay A., Fejes E., Nagy F. Characterization of proteins that interact with the GTP-bound form of the regulatory GTPase Ran in Arabidopsis. Plant J 1997, 11:93-103.
56. Vernoud V., Horton A., Yang Z., Nielsen E. Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol 2003, 131:1191-1208.
57. Gatenby A., Viitanen P. Structural and functional aspects of chaperonin mediated protein folding. Annu Rev Plant Physiol Plant Mol Biol 1994, 45:469-491.
58. Gromadski K., Wieden H., Rodnina M. Kinetic mechanism of elongation factor Ts-catalyzed nucleotide exchange in elongation factor Tu. Biochemistry 2002, 41:162-169.
59. Yu Q., Wingender R., Schulz M., Baluska F., Goldbach H. Short-term boron deprivation induces increased levels of cytoskeletal proteins in Arabidopsis roots. Plant Biol 2001, 3:335-340.
60. Yu Q., Baluška F., Jasper F., Menzel D., Goldbach H. Short-term boron deprivation enhances levels of cytoskeletal proteins in maize, but not zucchini, root apices. Physiol Plant 2003, 117:270-278.
61. Gunning B., Hardham A. Microtubules. Annu Rev Plant Physiol 1982, 33:651-698.
62. Loomis W., Durst R. Chemistry and biology of boron. Biofactors 1992, 3:229-239.
63. Rawson H. The developmental stage during which boron limitation causes sterility in wheat genotypes and the recovery of fertility. Aust J Plant Physiol 1996, 23:709-717.
64. Behrendt U., Zoglauer K. Boron controls suspensor development in embryogenic cultures of Larix decidua. Physiol Plant 1996, 97:321-326.
65. Bollaños L., de Esteban E., Lorenzo C., Fernandéz-Pascual M., de Felipe M., Gárate A., et al. Essentiality of boron for symbiotic dinitrogen fixation in pea (Pisum sativum)-Rhizobium nodules. Plant Physiol 1994, 104:85-90.
66. Salzer P., Bonanami A., Beyer K., Vögeli-Lange R., Aeschbacher R., Lange J., et al. Differential expression of eight chitinase genes in Medicago truncatula roots during mycorrhiza formation, nodulation and pathogen infection. Mol Plant-Microbe Interact 2000, 13:763-777.
67. Wan X.Y., Yu J.Y. Comparative proteomics analysis reveals an intimate protein network provoked by hydrogen peroxide stress in rice seedling leaves. Mol Cell Proteomics 2008, 7:1469-1488.
68. Ytterberg A., Jensen O. Modification-specific proteomics in plant biology. J Proteomics 2010, 73:2249-2266.
69. Bonilla I., Blevins D., Bolaños L. Boron functions in plants: looking beyond the cell wall. Plant physiology 2009, Sinauer Associates, Inc, Sunderland, MA. L. Taiz, E. Zeiger (Eds.).