Redox states of glutathione and ascorbate in root tips of poplar (Populus tremula×P. alba) depend on phloem transport from the shoot to the roots

Journal of Experimental Botany

Volumn 61, Issue 4, 2010, Pages 1065-1074

  Herschbach, Cornelia ^a   Scheerer, Ursula ^a   Rennenberg, Heinz ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Ascorbate; Glutathione; Phloem transport; Poplar; Redox state; Root growth

Indexed keywords

ASCORBIC ACID; GLUTATHIONE;

ARTICLE; ASPEN; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OXIDATION REDUCTION REACTION; PHLOEM; PLANT; PLANT ROOT; TRANSPORT AT THE CELLULAR LEVEL;

ASCORBIC ACID; BIOLOGICAL TRANSPORT; GLUTATHIONE; OXIDATION-REDUCTION; PHLOEM; PLANT ROOTS; PLANT SHOOTS; POPULUS;

POPULUS;

EID: 77649268108     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erp371     Document Type: Article

References (62)

1. 32P translocation in the phloem. American Journal of Botany 43, 143-148.
2. Bonas U, Schmitz K, Rennenberg H, Bergmann L. 1982. Phloem transport of sulphur in Ricinus. Planta 155, 82-88.
3. Bourgis F, Roje S, Nuccio ML, et al. 1999. S-Methylmethionine plays a major role in phloem sulphur transport and is synthesized by a novel type of methyltransferases. The Plant Cell 11, 1485-1497.
4. Brunold C. 1990. Reduction of sulfate to sulphide. In: Rennenberg H, Brunold C, De Kok LJ, Stulen I, eds. Sulphur nutrition and sulphur assimilation in higher plants. The Hague: SPB Academic Publishing, 13-31.
5. Cobbett CS, May MJ, Howden R, Rolls B. 1998. The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in c-glutamylcysteine synthetase. The Plant Journal 16, 73-78.
6. Conklin PL, Pallanca JE, Last RL, Smirnoff N. 1997. L-Ascorbic acid metabolism in the ascorbate-deficient Arabidopsis mutant vtc1. Plant Physiology 115, 1277-1285.
7. de Pinto MC, Francis D, De Gara L. 1999. The redox state of the ascorbate-dehydroascorbate pair as a specific sensor of cell division in tobacco BY-2 cells. Protoplasma 209, 90-97.
8. Foreman J, Demidchik V, Bothwell JHF, et al. 2003. Reactive oxygen species produced by NADPH oxidase regulated plant cell growth. Nature 422, 442-446.
9. Foyer CH, Halliwell B. 1976. The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133, 21-25.
10. Foyer CH, Noctor G. 2009. Redox regulation in photosynthetic organisms: signalling, acclimation, and practical implications. Antioxidants and Redox Signalling 11, 861-905.
11. Franceschi VR, Tarlyn NM. 2002. L-Ascorbic acid is accumulated in source leaf phloem and transported to sink tissues in plants. Plant Physiology 130, 649-656.
12. Fricker MD, May M, Meyer AJ, Sheard N, Whithe NS. 2000. Measurements of glutathione levels in intact roots of Arabidopsis. Journal of Microscopy 198, 162-173.
13. Groten K, Vanacker H, Dutilleul C, Bastian F, Bernard S, Carzaniga R, Foyer CH. 2005. The roles of redox processes in pea nodule development and senescence. Plant, Cell and Environment 28, 1293-1304.
14. 3 concentrations in a free-air exposure system. Plant Biology 9, 215-226.
15. Halliwell B. 2006. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiology 141, 312-322.
16. Hancock RD, NcRae D, Haupt S, Viola R. 2003. Synthesis of L-ascorbic acid in the phloem. BMC Plant Biology 3, 7.
17. Hartmann T, Mult S, Suter M, Rennenberg H, Herschbach C. 2000. Leaf age-dependent differences in sulphur assimilation and allocation in poplar (Populus tremula3P. alba) leaves. Journal of Experimental Botany 51, 1077-1088.
18. Herschbach C, Jouanin L, Rennenberg H. 1998. Overexpression of c-glutamylcysteine synthetase, but not glutathione synthetase, elevates glutathione allocation in the phloem of transgenic poplar trees. Plant and Cell Physiology 39, 447-451.
19. Herschbach C, Rennenberg H. 1996. Storage and remobilization of sulphur in beech trees (Fagus sylvatica). Physiologia Plantarum 98, 125-132.
20. 2S. Plant Physiology 124, 461-473.
21. Howden R, Andersen CR, Goldsbrough PB, Cobbett CS. 1995. Cadmium sensitive, glutathione deficient mutant of Arabidopsis thaliana. Plant Physiology 107, 1067-1073.
22. Hsu C-Y, Liu Y, Luthe DS, Yuceer C. 2006. Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. The Plant Cell 18, 1846-1861.
23. Jiang K, Feldman LJ. 2005. Regulation of apical meristem development. Annual Review of Cell and Developmental Biology 21, 485-509.
24. Jiang K, Meng YL, Feldman LJ. 2003. Quiescent centre formation in maize roots is associated with an auxin-regulated oxidizing environment. Development 130, 1429-1438.
25. Kato N, Esaka M. 1999. Changes in ascorbate oxidase gene expression and ascorbate levels in cell division and cell elongation in tobacco cells. Physiologia Plantarum 105, 321-329.
26. Kerk NM, Feldman LJ. 1995. A biochemical model for the initiation and maintenance of the quiescent centre: implications for organization of root meristem. Development 121, 2825-2833.
27. Kopriva S, Jones S, Koprivova A, Suter M, von Ballmoos P, Brander K, Flückiger J, Brunold C. 2001. Influence of chilling stress on the intercellular distribution of assimilatory sulphate reduction and thiols in Zea mays. Plant Biology 3, 24-31.
28. Kopriva S, Koprivova A. 2004. Plant adenosine 5#-phosphosulphate reductase: the past, the present, and the future. Journal of Experimental Botany 55, 1775-1783.
29. Kotchoni SO, Larrimore KE, Mukherjee M, Kempinski CF, Barth C. 2009. Alterations in the endogenous ascorbic acid content affect flowering time in Arabidopsis. Plant Physiology 149, 803-815.
30. Kuzuhara Y, Isobe A, Awazuhara M, Fujiwara T, Hayashi H. 2000. Glutathione levels in phloem sap of rice plants under sulphur deficient conditions. Soil Science and Plant Nutrition 46, 265-270.
31. 2- uptake in intact canola. Plant Physiology 111, 147-157.
32. Lee Y, Kim MW, Kim SH. 2007. Cell type identity in Arabidopsis roots is altered by both ascorbic acid-induced changes in the redox environment and the resultant endogenous auxin response. Journal of Plant Biology 50, 484-489.
33. 1 to S phase. New Phytologist 110, 469-471.
34. Liso R, De Tullio MC, Ciraci S, Balestrini R, La Rocca N, Bruno L, Chiappetta A, Bitonti B, Bonfante P, Arrigoni O. 2004. Localisation of ascorbic acid, ascorbic acid oxidase, and glutathione in roots of Cucurbita maxima L. Journal of Experimental Botany 55, 2589-2597.
35. Martin MN, Tarczynski MC, Shen B, Leustek T. 2005. The role of 5#adenylylsulfate reductase in controlling sulfate reduction in plants. Photosynthesis Research 86, 309-323.
36. Mason TG, Maskell EJ. 1928. Studies on the transport of carbohydrates in the cotton plant. I. A study of diurnal variation in the carbohydrates of leaf, bark, and wood, and of the effects of ringing. Annals of Botany 42, 189-253.
37. Matamoros MA, Loscos J, Coronado MJ, Ramos J, Sato S, Testillano PS, Tabata S, Becana M. 2006. Biosynthesis of ascorbic acid in legume root nodules. Plant Physiology 141, 1068-1077.
38. May MJ, Vernoux T, Leaver C, Van Montagu M, InzéD. 1998. Glutathione homeostasis in plants: implications for environmental sensing and plant development. Journal of Experimental Botany 49, 649-667.
39. Meyer AJ. 2008. The integration of glutathione homeostasis and redox signaling. Journal of Plant Physiology 165, 1390-1403.
40. Meyer AJ, Hell R. 2005. Glutathione homeostasis and redox-regulation by sulfhydryl groups. Photosynthesis Research 86, 435-457.
41. Mullineaux PM, Rausch T. 2005. Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynthesis Research 86, 459-474.
42. Noctor G. 2006. Metabolic signalling in defence and stress: the central roles of soluble redox couples. Plant, Cell and Environment 29, 409-425.
43. Noctor G, Foyer CH. 1998. Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249-279.
44. Noctor G, Strohm M, Jouanin L, Kunert K-J, Foyer CH, Rennenberg H. 1996. Synthesis of glutathione in leaves of transgenic poplar overexpressing c-glutamylcysteine synthetase. Plant Physiology 112, 1071-1078.
45. Ogawa K, Hatano-Iwasaki A, Yanagida M, Iwabuchi M. 2004. Level of glutathione is regulated by ATP-dependent ligation of glutamate and cysteine through photosynthesis in Arabidopsis thaliana: mechanism of strong interaction of light intensity with flowering. Plant and Cell Physiology 45, 1-8.
46. Okamura M. 1980. An improved method for determination of L-ascorbic acid and L-dehydroascorbic acid in blood plasma. Clinica et Chimica Acta 103, 259-268.
47. Olmos E, Kiddle G, Pellny TK, Kumar S, Foyer CH. 2006. Modulation of plant morphology, root architecture, and cell structure by low vitamin C in Arabidopsis thaliana. Journal of Experimental Botany 57, 1645-1655.
48. Pallanca JE, Smirnoff N. 2000. The control of ascorbic acid synthesis and turnover in pea seedlings. Journal of Experimental Botany 51, 669-674.
49. Polle A, Chakrabarti K, Schürmann W, Rennenberg H. 1990. Composition and properties of hydrogen peroxide decomposition systems in extracellular and total extracts from needles of Norway spruce (Picea abies L., Karst). Plant Physiology 94, 312-319.
50. Potters G, De Gara L, Asard H, Horemans N. 2002. Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiology and Biochemistry 40, 537-548.
51. Potters G, Horemans N, Bellone S, Caubergs RJ, Trost P, Guisez Y, Asard H. 2004. Dehydroascorbate influences the plant cell cycle through a glutathione-independent reduction mechanism. Plant Physiology 134, 1479-1487.
52. Rennenberg H, Herschbach C, Haberer K, Kopriva S. 2007. Sulphur metabolism in plants: are trees different? Plant Biology 9, 620-637.
53. Rennenberg P, Polle A. 1994. Metabolic consequences of atmospheric sulfur influx into plants. In: Alscher R, Wellburn AR, eds. Plants responses to the gaseous environment. Molecular, metabolic and physiological aspects. London: Chapman and Hall, 165-180.
54. Rennenberg H, Schmitz K, Bergmann L. 1979. Long-distance transport of sulphur in Nicotiana tabacum. Planta 147, 57-62
55. Sánchez-Fernández R, Fricker M, Corben LB, White NS, Sheard N, Leaver CJ, Van Montagu M, InzéD, May MJ. 1997. Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proceedings of National Academy of Sciences, USA 94, 2745-2750.
56. Scheerer U, Haensch R, Mendel R, Kopriva S, Rennenberg H, Herschbach C. 2009. Sulphur flux through the sulphate assimilation pathway is differently controlled by adenosine 5#-phosphosulphate reductase under stress and in transgenic poplar plants overexpressing c-ECS, SO or APR. Journal of Experimental Botany doi: 10.1093/jxb/ erp327.
57. 2. Plant, Cell and Environment 25, 1715-1727.
58. Schupp R, Rennenberg H. 1988. Diurnal changes in the glutathione concentration of spruce needles (Picea abies L.). Plant Science 57, 113-117.
59. Smirnoff N, Conklin PL, Loewus FA. 2001. Biosynthesis of ascorbic acid in plants: a renaissance. Annual Reviews of Plant Physiology and Plant Molecular Biology 52, 437-467.
60. Strohm M, Jouanin L, Kunert KJ, Pruvost C, Polle A, Foyer CH, Rennenberg H. 1995. Regulation of GSH synthesis in leaves of transgenic poplar (Populus tremula3P. alba) overexpressing GSH synthetase. The Plant Journal 7, 141-145.
61. Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krähenbühl U, Op den Camp R, Brunold C. 2002. Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5#-phosphosulfate reductase is more susceptible than ATP sulfurylase to negative control by thiols. The Plant Journal 31, 729-740.
62. Vernoux T, Wilson RC, Seeley KA, et al. 2000. The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. The Plant Cell 12, 97-109.