Early response of plant cell to carbon deprivation: In vivo31P-NMR spectroscopy shows a quasi-instantaneous disruption on cytosolic sugars, phosphorylated intermediates of energy metabolism, phosphate partitioning, and intracellular pHs

New Phytologist

Volumn 189, Issue 1, 2011, Pages 135-147

  Gout, Elisabeth ^a   Bligny, Richard ^a   Douce, Roland ^a   Boisson, Anne Marie ^a   Rivasseau, Corinne ^a  

^a CEA GRENOBLE   (France)

Author keywords

Cytosol vacuole; Hexose P; in vivo nuclear magnetic resonance (NMR) spectroscopy; Inorganic phosphate; Intracellular pHs; Plant cells; Sugar starvation

Indexed keywords

CARBON; PHOSPHATE;

CARBON; CYTOLOGY; CYTOPLASM; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PH; PHOSPHATE; PLASTID; SUCROSE;

ACER; ARTICLE; CARBOHYDRATE METABOLISM; CYTOSOL; ENERGY METABOLISM; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PH; PHOSPHORYLATION; PHYSIOLOGY; TIME;

ACER; CARBOHYDRATE METABOLISM; CARBON; CYTOSOL; ENERGY METABOLISM; HYDROGEN-ION CONCENTRATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHATES; PHOSPHORYLATION; TIME FACTORS;

ACER; ACER PSEUDOPLATANUS;

EID: 78649727709     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03449.x     Document Type: Article

References (55)

1. Antony E, Taybi T, Courbot M, Mugford ST, Smith JAC, Borland AM. 2008. Cloning, localization and expression analysis of vacuolar sugar transporters in the CAM plant Ananas comosus (pineapple). Journal of Experimental Botany 59: 1895-1908.
2. Aubert S, Bligny R, Douce R. 1996a. NMR studies of metabolism in cell suspensions and tissue cultures. In: Shachar-Hill Y, Pfeffer P, eds. Nuclear magnetic resonance in plant biology. Rockville, MD, USA: American Society of Plant Physiologists, 109-144.
3. 13C nuclear magnetic resonance. Journal of Experimental Botany 55: 2179-2189.
4. Aubert S, Gout E, Bligny R, Marty-Mazars D, Barrieu F, Alabouvette J, Marty F, Douce R. 1996b. Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates. The Journal of Cell Biology 133: 1251-1263.
5. Bligny R, Douce R. 1976. Les mitochondries de cellules végétales isolées (Acer pseudoplatanus L.) Physiologie Végétale 14: 499-515.
6. Bligny R, Leguay J-J. 1987. Techniques of cell suspension culture. Methods in Enzymology 148: 3-16.
7. Briskin DP, Thornley WR, Wyse RE. 1985. Membrane transport in isolated vesicles from sugar beet taproot. II. Evidence for a sucrose/H+-antiport. Plant Physiology 18: 865-870.
8. Brouquisse R, James F, Raymond P, Pradet A. 1992. Asparagine metabolism and nitrogen distribution during protein degradation in sugar-starved root tips. Planta 188: 384-395.
9. Bush DR. 1990. Electrogenicity, pH-dependence, and stoichiometry of the proton-sucrose symport. Plant Physiology 93: 1590-1596.
10. Büttner M. 2007. The monosaccharide transporter(-like) gene family in Arabidopsis. FEBS Letters 581: 2318-2324.
11. Cheng JG, Jones AM. 2004. AtRGS1 function in Arabidopsis thaliana. Methods in Enzymology 389: 338-350.
12. Cheng JG, Willard FS, Huang J, Liang J, Chasse SA, Jones AM, Siderovski DP. 2003. A seven-transmembrane RGS protein that modulates plant cell proliferation. Science 301: 1728-1731.
13. Chiou T-J, Bush DR. 1998. Sucrose is a signal molecule in assimilate partitioning. Proceedings of the National Academy of Sciences, USA 95: 4784-4788.
14. Contento AL, Kim S-J, Bassham DC. 2004. Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation. Plant Physiology 135: 2330-2347.
15. Devaux C, Baldet P, Joubès J, Dieuaide-Noubhani M, Just D, Chevallier C, Raymond P. 2003. Physiological, biochemical and molecular analysis of sugar-starvation responses in tomato roots. Journal of Experimental Botany 54: 1143-1151.
16. Dieuaide-Noubhani M, Canioni P, Raymond P. 1997. Sugar-starvation-induced changes of carbon metabolism in excised maize root tips. Plant Physiology 115: 1505-1513.
17. Dunn WA Jr. 1994. Autophagy and related mechanisms of lysosome-mediated protein degradation. Trends in Cell Biology 4: 139-143.
18. Endler A, Meyer S, Schelbert S, Schneider T, Weschke W, Peters SW, Keller F, Baginski S, Martinoia E, Schmidt UG. 2006. Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiology 141: 196-207.
19. Fernie AL, Martinoia E. 2009. Malate Jack of all trades or master of few? Phytochemistry 70: 828-832.
20. Genix P, Bligny R, Martin J-B, Douce R. 1990. Transient accumulation of asparagine in sycamore cells after a long period of sucrose starvation. Plant Physiology 94: 717-722.
21. + transport on the tonoplast of red beet (Beta vulgaris L.) storage tissue. Plant Physiology 107: 459-467.
22. Gout E, Bligny R, Douce R. 1992. Regulation of intracellular pH values in higher plant cells. The Journal of Biological Chemistry 267: 13903-13909.
23. 13C nuclear magnetic resonance studies of malate and citrate synthesis and compartmentation in higher plant cells. The Journal of Biological Chemistry 268: 3986-3992.
24. Gout E, Boisson A-M, Aubert S, Douce R, Bligny R. 2001. Origin of the cytoplasmic pH changes during anaerobic stress in higher plant cells. Carbon-13 and phosphorus-31 nuclear magnetic resonance studies. Plant Physiology 125: 912-925.
25. Hammond JP, White PJ. 2008. Sucrose transport in the phloem: integrating root responses to phosphorus starvation. The Journal of Experimental Botany 59: 93-109.
26. Jang J-C, León P, Zhou L, Sheen J. 1997. Hexokinase as a sugar sensor in higher plants. The Plant Cell 9: 5-19.
27. Journet E-P, Bligny R, Douce R. 1986. Biochemical changes during sucrose deprivation in higher plant cells. The Journal of Biological Chemistry 361: 3193-3199.
28. Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KG. 2007. Phosphate starvation responses are mediated by sugar signalling in Arabidopsis. Planta 225: 907-918.
29. Klionsky DJ, Ohsumi Y. 1999. Vacuolar import of proteins and organelles from the cytoplasm. Annual Review of Cell and Developmental Biology 15: 1-32.
30. Koch K. 2004. Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Current Opinion in Plant Biology 7: 235-246.
31. Kotoulas OB, Kalamidas SA, Kondomerkos DJ. 2006. Glycogen autophagy in glucose homeostasis. Pathology - Research and Practice 202: 631-638.
32. Lamport DTA. 1964. Cell suspension cultures of higher plants: isolation and growth energetics. Experimental Cell Research 33: 195-206.
33. Lee EJ, Koizumi N, Sano H. 2004. Identification of genes that are up-regulated in concert during sugar depletion in Arabidopsis. Plant, Cell & Environment 27: 337-345.
34. Lemoine R. 2000. Sucrose transporters in plants: update on function and structure. Biochimica et Biophysica Acta 1465: 246-262.
35. Li Y, Kharbanda S, Kufe D. 2009. MUC1 oncoprotein promotes autophagy in a survival response to glucose deprivation. International Journal of Oncology 34: 1691-1699.
36. Liu K, Tang Q, Fu C, Peng J, Yang H, Li Y, Hong H. 2007. Influence of glucose starvation on the pathway of death in insect cell line SI: apoptosis follows autophagy. Cytotechnology 54: 97-105.
37. 31P-NMR spectroscopy. FEBS Letters 242: 279-284.
38. +-pyrophosphatase. Biochimica et Biophysica Acta 1465: 37-51.
39. Martinoia E, Maeshima M, Neuhaus HE. 2007. Vacuolar transporters and their essential role in plant metabolism. Journal of Experimental Botany 58: 83-102.
40. Moore B, Zhou Li, Rolland P, Hall Q, Cheng W-H, Liu Y-X, Hwang I, Jones T, Sheen J. 2003. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300: 332-336.
41. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiologia Plantarum 15: 473-497.
42. Petersen OH, Michalak M, Verkhratsky A. 2005. Calcium signaling: past, present and future. Cell Calcium 38: 161-169.
43. 31P-nuclear magnetic resonance study using methylphosphonate as Pi analog. Plant Physiology 151: 1646-1657.
44. Rébeillé F, Bligny R, Martin J-B, Douce R. 1985. Effect of sucrose deprivation on sycamore (Acer pseudoplatanus) cell carbohydrate and Pi status. Biochemical Journal 226: 679-784.
45. 31P-nuclear magnetic resonance. Plant Physiology 113: 191-199.
46. Roberts JKM, Jardetzky O. 1981. Monitoring of cellular metabolism by NMR. Biochimica et Biophysica Acta 639: 53-76.
47. 31P NMR. Nature 283: 870-872.
48. Roby C, Martin J-B, Bligny R, Douce R. 1987. Biochemical changes during sucrose deprivation in higher plant cells. Phosphorus-31 nuclear magnetic resonance studies. The Journal of Biological Chemistry 262: 5000-5007.
49. Rolland F, Baena-Gonzales E, Sheen J. 2006. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annual Review of Plant Biology 57: 675-709.
50. Sanders D, Pelloux J, Brownlee C, Harper JF. 2002. Calcium at the crossroads of signaling. The Plant Cell 14: 401-417.
51. +-pumping ATPases: regulation and biosynthesis. The Plant Cell 11: 677-689.
52. Takeshige K, Baba M, Tsuboi S, Noda T, Ohsumi Y. 1992. Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. Journal of Cell Biology 119: 301-311.
53. Wormit A, Trentmann O, Feifer I, Lohr C, Tjaden J, Meyer S, Schmidt U, Martinoia E, Neuhaus HE. 2006. Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. The Plant Cell 18: 3476-3490.
54. Yu S-M. 1999. Cellular and genetic responses of plants to sugar starvation. Plant Physiology 121: 687-693.
55. Zell MB, Fahnenstich H, Maier A, Saigo M, Voznesenskaya EV, Edwards GE, Andreo C, Schleifenbaum F, Zell C, Drincovich MF et al. 2010. Analysis of Arabidopsis with highly reduced levels of malate and fumarate sheds light on the role of these organic acids as storage carbon molecules. Plant Physiology 152: 1251-1262.