Photosynthetic activity influences cellulose biosynthesis and phosphorylation of proteins involved therein in Arabidopsis leaves

Journal of Experimental Botany

Volumn 65, Issue 17, 2014, Pages 4997-5010

  Boex Fontvieille, Edouard ^a   Davanture, Marlène ^b   Jossier, Mathieu ^a   Zivy, Michel ^b   Hodges, Michael ^a   Tcherkez, Guillaume ^a,c  

^a INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^b INRA Institut National de la Recherche Agronomique   (France)

^c INSTITUT UNIVERSITAIRE DE FRANCE   (France)

Author keywords

Arabidopsis; Cellulose; Phosphoproteomics; Photosynthesis; Protein phosphorylation

Indexed keywords

ARABIDOPSIS;

ARABIDOPSIS PROTEIN; CELLULOSE;

ARABIDOPSIS; BIOSYNTHESIS; METABOLISM; PHOSPHORYLATION; PHOTOSYNTHESIS; PLANT LEAF;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELLULOSE; PHOSPHORYLATION; PHOTOSYNTHESIS; PLANT LEAVES;

EID: 84907419348     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru268     Document Type: Article

References (51)

1. Bathellier C, Tcherkez G, Mauve C, Bligny R, Gout E, Ghashghaie J. 2009. On the resilience of nitrogen assimilation by intact roots under starvation, as revealed by isotopic and metabolomic techniques. Rapid Communications in Mass Spectrometry 23, 2847-2856.
2. Bischoff V, Desprez T, Mouille G, Vernhettes S, Gonneau M, Höfte H. 2011. Phytochrome regulation of cellulose synthesis in Arabidopsis. Current Biology 21, 1822-1827.
3. Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJR. 2009. Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nature Protocols 4, 484-494.
4. Boesger J, Wagner V, Weisheit W, Mittag M. 2012. Application of phosphoproteomics to find targets of casein kinase 1 in the flagellum of chlamydomonas. International Journal of Plant Genomics 2012, 581460.
5. Boettger T, Haupt M, Knöller K et al., 2007. Wood cellulose preparation methods and mass spectrometric analyses of δ13C, δ18O, and nonexchangeable δ2H values in cellulose, sugar, and starch: An interlaboratory comparison. Analytical Chemistry 79, 4603-4612.
6. Boex-Fontvieille ERM, Davanture M, Jossier M, Zivy M, Hodges M, Tcherkez G. 2013. Photosynthetic control of Arabidopsis leaf cytoplasmic translation initiation by protein phosphorylation. Plos One 8, e70692.
7. Bonhomme L, Valot B, Tardieu F, Zivy M. 2012. Phosphoproteome dynamics upon changes in plant water status reveal early events associated with rapid growth adjustment in maize leaves. Molecular and Cellular Proteomics 11, 957-972.
8. Botanga CJ, Bethke G, Chen Z, Gallie DR, Fiehn O, Glazebrook J. 2012. Metabolite profiling of Arabidopsis inoculated with Alternaria brassicicola reveals that ascorbate reduces disease severity. Molecular Plant-Microbe Interactions 25, 1628-1638.
9. Bringmann M, Li E, Sampathkumar A, Kocabek T, Hauser MT, Persson S. 2012. POM-POM2/cellulose synthase interacting 1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24, 163-177.
10. Budde RJ, Randall DD. 1990. Light as a signal influencing the phosphorylation status of plant proteins. Plant Physiology 94, 1501-1504.
11. Canam T, Park J-Y, Yu K, Campbell M, Ellis D, Mansfield S. 2006. Varied growth, biomass and cellulose content in tobacco expressing yeast-derived invertases. Planta 224, 1315-1327.
12. Chen S, Ehrhardt DW, Somerville CR. 2010. Mutations of cellulose synthase (CESA1) phosphorylation sites modulate anisotropic cell expansion and bidirectional mobility of cellulose synthase. Proceedings of the National Academy of Sciences, USA 107, 17188-17193.
13. Coleman HD, Ellis DD, Gilbert M, Mansfield SD. 2006. Up-regulation of sucrose synthase and UDP-glucose pyrophosphorylase impacts plant growth and metabolism. Plant Biotechnology Journal 4, 87-101.
14. Dickson RE, Larson PR. 1975. Incorporation of 14C-photosynthate into major chemical fractions of source and sink leaves of cottonwood. Plant Physiology 56, 185-193.
15. Duff S, Chollet R. 1995. In vivo regulation of wheat-leaf phosphoenolpyruvate carboxylase by reversible phosphorylation. Plant Physiology 107, 775-782.
16. Echwald SM, Bach H, Vestergaard H, Richelsen B, Kristensen K, Drivsholm T, Borch-Johnsen K, Hansen T, Pedersen O. 2002. A P387L variant in protein tyrosine phosphatase-1B (PTP-1B) is associated with type 2 diabetes and impaired serine phosphorylation of PTP-1B in vitro. Diabetes 51, 1-6.
17. Escobar-Gutiérrez AJ, Gaudillère J-P. 1997. Carbon partitioning in source leaves of peach, a sorbitol-synthesizing species, is modified by photosynthetic rate. Physiologia Plantarum 100, 353-360.
18. Fernie AR, Willmitzer L. 2004. Carbohydrate metabolism, Handbook of plant biotechnology. New York: J. Wiley and Sons, Ltd.
19. Garton AJ, Tonks NK. 1994. PTP-PEST: a protein tyrosine phosphatase regulated by serine phosphorylation. EMBO Journal 13, 3763.
20. Gu Y, Kaplinsky N, Bringmann M, Cobb A, Carroll A, Sampathkumar A, Baskin TI, Persson S, Somerville CR. 2010. Identification of a cellulose synthase-associated protein required for cellulose biosynthesis. Proceedings of the National Academy of Sciences, USA 107, 12866-12871.
21. Gururaj A, Barnes CJ, Vadlamudi RK, Kumar R. 2004. Regulation of phosphoglucomutase 1 phosphorylation and activity by a signaling kinase. Oncogene 23, 8118-8127.
22. Hamann T, Osborne E, Youngs H, Misson J, Nussaume L, Somerville C. 2004. Global expression analysis of CESA and CSL genes in Arabidopsis. Cellulose 11, 279-286.
23. Harmer SL, Hogenesch JB, Straume M, Chang H-S, Han B, Zhu T, Wang X, Kreps JA, Kay SA. 2000. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110-2113.
24. Hatch MD, Slack CR. 1966. Photosynthesis by sugar-cane leaves. A new carboxylation reaction and the pathway of sugar formation. Biochemical Journal 101, 103-111.
25. Hochberg Y, Benjamini Y. 1990. More powerful procedures for multiple significance testing. Statistics in medicine 9, 811-818.
26. Huber JL, Huber SC. 1992. Site-specific serine phosphorylation of spinach leaf sucrose-phosphate synthase. Biochemical Journal 283, 877-882.
27. Huber SC, Huber JL. 1996. Role and regulation of sucrose-phosphate synthase in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 431-444.
28. Hue L, Rider MH. 1987. Role of fructose 2,6-bisphosphate in the control of glycolysis in mammalian tissues. Biochemical Journal 245, 313-324.
29. Joshi CP, Mansfield SD. 2007. The cellulose paradox - simple molecule, complex biosynthesis. Current Opinion in Plant Biology 10, 220-226.
30. Konishi T, Ohmiya Y, Hayashi T. 2004. Evidence that sucrose loaded into the phloem of a poplar leaf is used directly by sucrose synthase associated with various beta-glucan synthases in the stem. Plant Physiology 134, 1146-1152.
31. Lan P, Li W, Wen TN, Schmidt W. 2012. Quantitative phosphoproteome profiling of iron-deficient Arabidopsis roots. Plant Physiology 159, 403-417.
32. Li S, Lei L, Somerville CR, Gu Y. 2012. Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes. Proceedings of the National Academy of Sciences, USA 109, 185-190.
33. Liu J, Ning D, Zhao G, Cheng Y, Wang B. 2013. Large-scale analysis of protein phosphorylation in Populus leaves. Journal of Plant Biochemistry and Biotechnology : 1-11.
34. Loader NJ, Robertson I, Barker AC, Switsur VR, Waterhouse JS. 1997. An improved technique for the batch processing of small wholewood samples to cellulose. Chemical Geology 136, 313-317.
35. Lozovaya VV, Zabotina OA, Widholm JM. 1996. Synthesis and turnover of cell-wall polysaccharides and starch in photosynthetic soybean suspension cultures. Plant Physiology 111, 921-929.
36. Minor J. 1983. Nonfermentable, glucose-containing products formed from glucose under cellulose acid hydrolysis conditions. Journal of Applied Polymer Science: Applied Polymer Symposium 37, 617-629.
37. Nühse TS, Bottrill AR, Jones AME, Peck SC. 2007. Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. The Plant Journal 51, 931-940.
38. Pillonel C, Buchala A, Meier H. 1980. Glucan synthesis by intact cotton fibres fed with different precursors at the stages of primary and secondary wall formation. Planta 149, 306-312.
39. Ramon M, De Smet I, Vandesteene L, Naudts M, Leyman B, Van Dijck P, Rolland F, Beeckman T, Thevelein JM. 2009. Extensive expression regulation and lack of heterologous enzymatic activity of the class II trehalose metabolism proteins from Arabidopsis thaliana. Plant, Cell and Environment 32, 1015-1032.
40. Sharkey TD, Berry JA, Raschke K. 1985. Starch and sucrose synthesis in Phaseolus vulgaris as affected by light, CO2, and abscisic acid. Plant Physiology 77, 617-620.
41. Somerville C. 2006. Cellulose synthesis in higher plants. Annual Review of Cell and Developmental Biology 22, 53-78.
42. Stitt M, Herzog B, Heldt HW. 1984a. Control of photosynthetic sucrose synthesis by fructose-2,6-bisphosphate. I. Coordination of CO2 fixation and sucrose synthesis. Plant Physiology 75, 548-553.
43. Stitt M, Kürzel B, Heldt HW. 1984b. Control of photosynthetic sucrose synthesis by fructose-2,6-bisphosphate. II. Partitioning between sucrose and starch. Plant Physiology 75, 554-560.
44. Stitt M, Wirtz W, Heldt HW. 1983. Regulation of sucrose synthesis by cytoplasmic fructosebisphosphatase and sucrose phosphate synthase during photosynthesis in varying light and carbon dioxide. Plant Physiology 72, 767-774.
45. Stitt M, Zeeman SC. 2012. Starch turnover: pathways, regulation and role in growth. Current Opinion in Plant Biology 15, 282-292.
46. Takeuchi Y, Kondo N. 1988. Effect of abscisic acid on cell-wall metabolism in guard cells of Vicia faba L. Plant and Cell Physiology 29, 573-580.
47. Tan YD, Xu H. 2014. A general method for accurate estimation of false discovery rates in identification of differentially expressed genes. Bioinformatics doi: 10.1093/bioinformatics/btu124.
48. Tetlow IJ, Morell MK, Emes MJ. 2004. Recent developments in understanding the regulation of starch metabolism in higher plants. Journal of Experimental Botany 55, 2131-2145.
49. Toroser D, Huber SC. 1997. Protein phosphorylation as a mechanism for osmotic-stress activation of sucrose-phosphate synthase in spinach leaves. Plant Physiology 114, 947-955.
50. Valot B, Langella O, Nano E, Zivy M. 2011. MassChroQ: a versatile tool for mass spectrometry quantification. Proteomics 11, 3572-3577.
51. Wiese A, Christ MM, Virnich O, Schurr U, Walter A. 2007. Spatiotemporal leaf growth patterns of Arabidopsis thaliana and evidence for sugar control of the diel leaf growth cycle. New Phytologist 174, 752-761.