Exogenous application of 5-aminolevulinic acid increases the transcript levels of sulfur transport and assimilatory genes, sulfate uptake, and cysteine and glutathione contents in Arabidopsis thaliana

Soil Science and Plant Nutrition

Volumn 56, Issue 2, 2010, Pages 281-288

  Maruyama Nakashita, Akiko ^a,b,c   Hirai, Masami Yokota ^b   Funada, Shigeyuki ^c   Fueki, Shoichi ^c,d  

^a FUKUI PREFECTURAL UNIVERSITY   (Japan)

^b RIKEN Plant Science Center   (Japan)

^c R and D Center Research and Safety and Technology Management Unit   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

Author keywords

5 aminolevulinic acid; Arabidopsis thaliana; Cysteine; Glutathione; Sulfate uptake

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 77953218094     PISSN: 00380768     EISSN: 17470765     Source Type: Journal    
DOI: 10.1111/j.1747-0765.2010.00458.x     Document Type: Article

References (42)

1. Askira Y, Rubin B, Rabinowitch HD. Differential response to the herbicidal activity of δ-aminolevulinic acid in plant with high and low sod activity. Free Radic. Res. Commun 1991, 12-13:837-843.
2. Chakraborty N, Tripathy BC. Involvement of singlet oxygen in 5-aminolevulinic acid-induced photodynamic damage of cucumber (Cucumis sativus L.) chloroplasts. Plant Physiol. 1992, 98:7-11.
3. Crawford NM, Kahn ML, Leustek T, Long SR. Nitrogen and sulfur. Biochemistry & Molecular Biology of Plants 2000, 824-849. Buchanan BB, Gruissem W, Jones RL, Eds, pp, American Society of Plant Biologists, Rockville, MD
4. Foyer CH, Theodoulou FL, Delrot S. The functions of inter- and intracellular glutathione transport systems in plants. Trends Plant Sci. 2001, 6:486-492.
5. Gutierrez-Marcos JF, Roberts MA, Campbell EI, Wray JL. Three members of a novel small gene-family from Arabidopsis thaliana able to complement functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and " APS reductase" activity. Proc. Natl Acad. Sci. USA 1996, 93:13377-13382.
6. Herschbach C, Jouanin L, Rennenberg H. Overexpression of {gamma}-glutamylcysteine synthetase, but not of glutathione synthetase, elevates glutathione allocation in the phloem of transgenic poplar trees. Plant Cell Physiol. 1998, 39:447-451.
7. Hicks LM, Cahoon RE, Bonner ER, Rivard RS, Sheffield J, Jez JM. Thiol-based regulation of redox-active glutamate-cysteine ligase from Arabidopsis thaliana. Plant Cell 2007, 19:2653-2661.
8. Hirai MY, Fujiwara T, Awazuhara M, Kimura Y, Noji M, Saito K. Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J. 2003, 33:651-663.
9. Hirai MY, Fujiwara T, Chino M, Naito S. Effects of sulfate concentrations on the expression of a soybean seed storage protein gene and its reversibility in transgenic Arabidopsis thaliana. Plant Cell Physiol. 1995, 36:1331-1339.
10. Hotta Y, Tanaka T, Takaoka H, Takeuchi Y, Konnai M. New physiological effects of 5-aminolevulinic acid in plants: The increase of photosynthesis, chlorophyll content, and plant growth. Biosci. Biotechnol. Biochem. 1997a, 61:2025-2028.
11. Hotta Y, Tanaka T, Takaoka H, Takeuchi Y, Konnai M. Promotive effects of 5-aminolevulinic acid on the yield of several crops. Plant Growth Regul. 1997b, 22:109-114.
12. Kataoka T, Watanabe-Takahashi A, Hayashi N. Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 2004, 16:2693-2704.
13. Kawashima CG, Berkowitz O, Hell R, Noji M, Saito K. Characterization and expression analysis of a serine acetyltransferase gene family involved in a key step of the sulfur assimilation pathway in Arabidopsis. Plant Physiol. 2005, 137:220-230.
14. Kittsteiner U, Mostowska A, Redinger W. The greening process in cress seedlings. I. Pigment accumulation and ultrastructure after application of 5-aminolevulinate and complexing agents. Physiol. Plant. 1991, 81:139-147.
15. Kopriva S, Muheim R, Koprivova A. Light regulation of assimilatory sulphate reduction in Arabidopsis thaliana. Plant J. 1999, 20:37-44.
16. Koprivova A, North KA, Kopriva S. Complex signaling network in regulation of adenosine 5′-phosphosulfate reductase by salt stress in Arabidopsis roots. Plant Physiol. 2008, 146:1408-1420.
17. Koprivova A, Suter M, Op den Camp R, Brunold C, Kopriva S. Regulation of sulfur assimilation by nitrogen in Arabidopsis. Plant Physiol. 2000, 122:737-746.
18. Kumaran S, Yi H, Krishnan HB, Jez JM. Assembly of the cysteine synthase complex and the regulatory role of protein-protein interactions. J. Biol. Chem. 2009, 284:10268-10275.
19. Lappartient AG, Vidmar JJ, Leustek T, Glass ADM, Touraine B. Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J. 1999, 18:89-95.
20. Leustek T, Martin MN, Bick J, Davies JP. Pathways and regulation of sulfur metabolism revealed through molecular genetic studies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2000, 51:141-166.
21. Li Y, Dankher OP, Carreira L, Smith AP, Meagher RB. The shoot-specific expression of gamma-glutamylcysteine synthetase directs the long-distance transport of thiol-peptides to roots conferring tolerance to mercury and arsenic. Plant Physiol. 2006, 141:288-298.
22. Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H. A novel regulatory pathway of sulfate uptake in Arabidopsis roots: implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. Plant J. 2004a, 38:779-789.
23. Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H. Regulation of high-affinity sulfate transporters in plants: towards systematic analysis of sulfur signaling and regulation. J. Exp. Bot. 2004b, 55:1843-1849.
24. Mishra SN, Srivastava HS. Stimulation of nitrate reductase activity by delta amino levulinic acid in excised maize leaves. Cell. Mol. Life Sci. 1983, 39:1118-1120.
25. Noctor G, Foyer CH. ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998, 49:249-279.
26. Noctor G, Gomez L, Vanacker H, Foyer CH. Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J. Exp. Bot. 2002, 53:1283-1304.
27. Rauser WE, Schupp R, Rennenberg H. Cysteine, [gamma}-glutamylcysteine, and glutathione levels in maize seedlings. Distribution and translocation in normal and cadmium-exposed plants. Plant Physiol. 1991, 97:128-138.
28. Rebeiz CA, Reddy KN, Nandihalli UB, Velu J. Tetrapyrrole-dependent photodynamic herbicides. Photochem. Photobiol. 1990, 52:1099-1117.
29. Saito K. Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol. 2004, 136:2443-2450.
30. Shibagaki N, Rose A, McDermott JP. Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J. 2002, 29:475-486.
31. Smith FW, Ealing PM, Hawkesford MJ, Clarkson DT. Plant members of a family of sulfate transporters reveal functional subtypes. Proc. Natl Acad. Sci. USA 1995, 92:9373-9377.
32. Smith FW, Hawkesford MJ, Ealing PM. Regulation of expression of a cDNA from barley roots encoding a high affinity sulfate transporter. Plant J. 1997, 12:875-884.
33. Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K. The roles of three functional sulfate transporters involved in uptake and translocation of sulfate in Arabidopsis thaliana. Plant J. 2000, 23:171-182.
34. Takahashi H, Yamazaki M, Sasakura N. Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate starved roots plays a central role in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 1997, 94:11102-11107.
35. Tanaka T, Iwai K, Watanabe K, Hotta Y. Development of 5-aminolevulinic acid for agricultural uses. Regul. Plant Growth Dev. 2005, 40:22-29.
36. Tausza M, Pilcha B, Rennenberg H, Grilla D, Herschbach C. Root uptake, transport, and metabolism of externally applied glutathione in Phaseolus vulgaris seedlings. J. Plant Physiol. 2004, 161:347-349.
37. Vauclare P, Kopriva S, Fell D. Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J. 2002, 31:729-740.
38. Vidmar JJ, Tagmount A, Cathala N, Touraine B, Davidian JCE. Cloning and characterization of a root specific high-affinity sulfate transporter from Arabidopsis thaliana. FEBS Lett. 2000, 475:65-69.
39. Wang R, Okamoto M, Xing X, Crawford N. Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol. 2003, 132:556-567.
40. Wirtz M, Hell R. Dominant-negative modification reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. Plant Cell 2007, 19:625-639.
41. Yoshimoto N, Inoue E, Watanabe-Takahashi A, Saito K, Takahashi H. Posttranscriptional regulation of high-affinity sulfate tansporters in Arabidopsis by sulfur nutrition. Plant Physiol. 2007, 145:378-388.
42. Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K. Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J. 2002, 29:465-473.