Absolute quantification of Medicago truncatula sucrose synthase isoforms and N-metabolism enzymes in symbiotic root nodules and the detection of novel nodule phosphoproteins by mass spectrometry

Journal of Experimental Botany

Volumn 59, Issue 12, 2008, Pages 3307-3315

  Wienkoop, Stefanie ^a   Larrainzar, Estíbaliz ^b   Glinski, Mirko ^a   González, Esther M ^b   Arrese Igor, Cesar ^b,c   Weckwerth, Wolfram ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b PUBLIC UNIVERSITY OF NAVARRE   (Spain)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

Absolute quantification; Alkaline invertase; Asparagine synthetase; De novo sequencing; Mass western; Medicago truncatula; Phosphoproteomics; Plant proteomics; Root nodules; Stable isotope labelling; Sucrose synthase

Indexed keywords

GLUCOSYLTRANSFERASE; ISOPROTEIN; NITROGEN; PHOSPHOPROTEIN; SUCROSE SYNTHASE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BARREL MEDIC; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; NODULATION; PHOSPHORYLATION; PHYSIOLOGY; SEQUENCE HOMOLOGY; SYMBIOSIS;

AMINO ACID SEQUENCE; GENE EXPRESSION REGULATION, PLANT; GLUCOSYLTRANSFERASES; MASS SPECTROMETRY; MEDICAGO TRUNCATULA; MOLECULAR SEQUENCE DATA; NITROGEN; PHOSPHOPROTEINS; PHOSPHORYLATION; PLANT PROTEINS; PROTEIN ISOFORMS; ROOT NODULES, PLANT; SEQUENCE HOMOLOGY, AMINO ACID; SYMBIOSIS;

MEDICAGO TRUNCATULA;

EID: 51749100872     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ern182     Document Type: Article

References (39)

1. Alexander RD, Morris PC. 2006. A proteomic analysis of 14-3-3 binding proteins from developing barley grains. Proteomics 6, 1886-1896.
2. Antunes F, Aguilar M, Pineda M, Sodek L. 2008. Nitrogen stress and the expression of asparagine synthetase in roots and nodules of soybean (Glycine max L. Merr.). Physiologia Plantarum 133, 736-743.
3. Duncan KA, Hardin SC, Huber SC. 2006. The three maize sucrose synthase isoforms differ in distribution, localization, and phosphorylation. Plant and Cell Physiology 47, 959-971.
4. Duncan KA, Huber SC. 2007. Sucrose synthase oligomerization and F-actin association are regulated by sucrose concentration and phosphorylation. Plant and Cell Physiology 48, 1612-1623.
5. Flemetakis E, Efrose RC, Ott T, Stedel C, Aivalakis G, Udvardi MK, Katinakis P. 2006. Spatial and temporal organization of sucrose metabolism in Lotus japonicus nitrogen-fixing nodules suggests a role for the elusive alkaline/neutral invertase. Plant Molecular Biology 62, 53-69.
6. Glinski M, Weckwerth W. 2005. Differential multisite phosphorylation of the trehalose-6-phosphate synthase gene family in Arabidopsis thaliana: a mass spectrometry-based process for multiparallel peptide library phosphorylation analysis. Molecular and Cellular Proteomics 4, 1614-1625.
7. Gonzalez EM, Gordon AJ, James CL, Arrese-Igor C. 1995. The role of sucrose synthase in the response of soybean nodules to drought. Journal of Experimental Botany 46, 1515-1523.
8. Gordon AJ, Minchin FR, James CL, Komina O. 1999. Sucrose synthase in legume nodules is essential for nitrogen fixation. Plant Physiology 120, 867-877.
9. 2 fixation are related to nodule sucrose synthase activity. Plant Physiology 114, 937-946.
10. Hardin SC, Tang GQ, Scholz A, Holtgraewe D, Winter H, Huber SC. 2003. Phosphorylation of sucrose synthase at serine 170: occurrence and possible role as a signal for proteolysis. The Plant Journal 35, 588-603.
11. Hardin SC, Winter H, Huber SC. 2004. Phosphorylation of the amino terminus of maize sucrose synthase in relation to membrane association and enzyme activity. Plant Physiology 134, 1427-1438.
12. Hohnjec N, Becker JD, Puhler A, Perlick AM, Küster H. 1999. Genomic organization and expression properties of the MtSucS1 gene, which encodes a nodule-enhanced sucrose synthase in the model legume Medicago truncatula. Molecular and General Genetics 261, 514-522.
13. Hohnjec N, Perlick AM, Puhler A, Küster H. 2003. The Medicago truncatula sucrose synthase gene MtSucS1 is activated both in the infected region of root nodules and in the cortex of roots colonized by arbuscular mycorrhizal fungi. Molecular Plant-Microbe Interactions 16, 903-915.
14. Horst I, Welham T, Kelly S, Kaneko T, Sato S, Tabata S, Parniske M, Wang TL. 2007. TILLING mutants of Lotus japonicus reveal that nitrogen assimilation and fixation can occur in the absence of nodule-enhanced sucrose synthase. Plant Physiology 144, 806-820.
15. Huber SC, Huber JL, Liao PC, Gage DA, McMichael RW, Chourey PS, Hannah LC, Koch K. 1996. Phosphorylation of serine-15 of maize leaf sucrose synthase: occurrence in vivo and possible regulatory significance. Plant Physiology 112, 793-802.
16. Huber TA, Streeter JG. 1985. Purification and properties of asparagine synthetase from soybean root-nodules. Plant Science 42, 9-17.
17. Hummel J, Niemann M, Wienkoop S, Schulze W, Steinhauser D, Selbig J, Walther D, Weckwerth W. 2007. ProMEX: a mass spectral reference database for proteins and protein phosphorylation sites. BMC Bioinformatics 8, 216.
18. Joy KW, Ireland RJ, Lea PJ. 1983. Asparagine synthesis in pea leaves and the occurrence of an asparagine synthetase inhibitor. Plant Physiology 73, 165-168.
19. Komina O, Zhou Y, Sarath G, Chollet R. 2002. In vivo and in vitro phosphorylation of membrane and soluble forms of soybean nodule sucrose synthase. Plant Physiology 129, 1664-1673.
20. Kuster H, Vieweg MF, Manthey K, Baier MC, Hohnjec N, Perlick AM. 2007. Identification and expression regulation of symbiotically activated legume genes. Phytochemistry 68, 8-18.
21. Larrainzar E, Wienkoop S, Weckwerth W, Ladrera R, Arrese-Igor C, Gonzalez EM. 2007. Medicago truncatula root nodule proteome analysis reveals differential plant and bacteroid responses to drought stress. Plant Physiology 144, 1495-1507.
22. Lea PJ, Sodek L, Parry MAJ, Shewry PR, Halford NG. 2007. Asparagine in plants. Annals of Applied Biology 150, 1-26.
23. Lehmann U, Wienkoop S, Weckwerth W. 2008. If the antibody fails: a mass western approach. The Plant Journal doi: 10.1111/j.1365-313X.2008. 03554.x.
24. Lima L, Seabra A, Melo P, Cullimore J, Carvalho H. 2006. Post-translational regulation of cytosolic glutamine synthetase of Medicago truncatula. Journal of Experimental Botany 57, 2751-2761.
25. Mallick P, Schirle M, Chen SS, Flory MR, Lee H, Martin D, Raught B, Schmitt R, Werner T, Kuster B, Aebersold R. 2007. eComputational prediction of proteotypic peptides for quantitative proteomics. Nature Biotechnology 25, 125-131.
26. Marino D, Hohnjec N, Küster H, Moran JF, Gonzalez EM, Arrese-Igor C. 2008. Evidence for transcriptional and posttranscriptional regulation of sucrose synthase in pea nodules by the cellular redox state. Molecular Plant-Microbe Interactions 21, 622-630.
27. Mazanek M, Mituloviae G, Herzog F, Stingl C, Hutchins JR, Peters JM, Mechtler K. 2007. Titanium dioxide as a chemoaffinity solid phase in offline phosphopeptide chromatography prior to HPLC-MS/MS analysis. Nature Protocols 2, 1059-1069.
28. Morell M, Copeland L. 1984. Enzymes of sucrose breakdown in soybean nodules: alkaline invertase. Plant Physiology 74, 1030-1034.
29. Okamoto K, Akazawa T. 1980. Enzymic mechanism of starch breakdown in germinating rice seeds. 9. De novo synthesis of β-amylase. Plant Physiology 65, 81-84.
30. 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.
31. Shaw JR, Ferl RJ, Baier J, St Clair D, Carson C, McCarty DR, Hannah LC. 1994. Structural features of the maize sus1 gene and protein. Plant Physiology 106, 1659-1665.
32. Shevchenko A, Wilm M, Vorm O, Mann M. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Analytical Chemistry 68, 850-858.
33. Streeter JG. 1977. Asparaginase and asparagine transaminase in soybean leaves and root nodules. Plant Physiology 60, 235-239.
34. Vance CP. 2008. Carbon and nitrogen metabolism in legume nodules. In: Dilworth MJ, James EK, Sprent JI, Newton WE, eds. Nitrogen-fixing leguminous symbioses. New York: Springer-Verlag, 293-320.
35. Wienkoop S, Larrainzar E, Niemann M, Gonzalez EM, Lehmann U, Weckwerth W. 2006. Stable isotope-free quantitative shotgun proteomics combined with sample pattern recognition for rapid diagnostics. Journal of Separation Science 29, 2793-2801.
36. Wienkoop S, Weckwerth W. 2006. Relative and absolute quantitative shotgun proteomics: targeting low-abundance proteins in Arabidopsis thaliana. Journal of Experimental Botany 57, 1529-1535.
37. 2+-dependent protein kinase. FEBS Letters 410, 126-130.
38. Zhang XQ, Li B, Chollet R. 1995. In vivo regulatory phosphorylation of soybean-nodule phosphoenolpyruvate carboxylase. Plant Physiology 108, 1561-1568.
39. Zhang XQ, Lund AA, Sarath G, Cerny RL, Roberts DM, Chollet R. 1999. Soybean nodule sucrose synthase (Nodulin-100): further analysis of its phosphorylation using recombinant and authentic root-nodule enzymes. Archives of Biochemistry and Biophysics 371, 70-82.