Using a suppression subtractive library-based approach to identify tobacco genes regulated in response to short-term sulphur deficit

Journal of Experimental Botany

Volumn 56, Issue 416, 2005, Pages 1575-1590

  Wawrzyńska, Anna ^a   Lewandowska, Małgorzata ^a   Hawkesford, Malcolm J ^b   Sirko, Agnieszka ^a  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^b ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

Starvation; Stress signaling; Sulphur metabolism; Suppression subtractive hybridization; Tobacco

Indexed keywords

DATA REDUCTION; DATABASE SYSTEMS; METABOLISM; MONITORING; PLANTS (BOTANY); STRESS ANALYSIS; SULFUR;

IMMATURE LEAVES; SULFUR DEFICIENCY; SULFURE METABOLISM; TOBACCO GENES;

GENES;

SULFUR; VEGETABLE PROTEIN;

ARTICLE; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; METHODOLOGY; PHYSIOLOGY; PLANT LEAF; PLANT ROOT; PLANT STEM; TOBACCO; UPREGULATION;

DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANT STEMS; SULFUR; TOBACCO; TRANSCRIPTION, GENETIC; UP-REGULATION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAGNOLIOPHYTA; NICOTIANA TABACUM; SOLANACEAE;

EID: 20044374360     PISSN: 00220957     EISSN: None     Source Type: Journal    
DOI: 10.1093/jxb/eri152     Document Type: Article

References (82)

1. Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G. 2003. Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. The Plant Cell 15, 439-447.
2. Ahn B-H, Lee J-H, Bae Y-S. 2003. Identification of mutations in protein kinase CKIIα subunit that affect its binding to ribosomal protein L41 and homodimerization. Journal of Biochemistry and Molecular Biology 36, 344-348.
3. Ball L, Accotto GP, Bechtold U, et al. 2004. Evidence for a direct link between glutathione biosynthesis and stress defence gene expression in Arabidopsis. The Plant Cell 16, 2448-2462.
4. Barakat A, Szick-Miranda K, Chang I-F, Guyot R, Blanc G, Cooke R, Delseny M, Baily-Serres J. 2001. The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome. Plant Physiology 127, 398-415.
5. Belenghi B, Acconcia F, Trovato M, Perazzolli M, Bocedi A, Polticelli F, Ascenzi P, Delledonne M. 2003. AtCYS1, a cystatin from Arabidopsis thaliana, suppresses hypersensitive cell death. European Journal of Biochemistry 270, 2593-2604.
6. Ben-Shem A, Frolow F, Nelson N. 2003. Crystal structure of plant photosystem I. Nature 426, 630-635.
7. Bocharov EV, Sobol AG, Pavlov KV, Korzhnev DM, Jaravine VA, Gudkov AT, Arseniev AS. 2004. From structure and dynamics of protein L7/L12 to molecular swiching in ribosome. Journal of Biological Chemistry 279, 17697-17706.
8. Bork C, Schwenn JD, Hell R. 1998. Isolation and characterization of a gene for assimilatory sulfite reductase from Arabidopsis thaliana. Gene 212, 147-153.
9. Breyne P, Dreesen R, Cannoot B, Rombaut D, Vandepoele K, Rombauts S, Vanderhaeghen R, Inzé D, Zabeau M. 2003. Quantitative cDNA-AFLP analysis for genome-wide expression studies. Molecular Genetics and Genomics 269, 173-179.
10. 2S and pedospheric sulfate nutrition. Plant Physiology 136, 3396-3408.
11. Castillejo C, de la Fuente JI, Iannetta P, Botella MA, Valpuesta V. 2004. Pectin esterase gene family in strawberry fruit: study of FaPE1, a ripening-specific isoform. Journal of Experimental Botany 55, 909-918.
12. Chandra Sanyal S, Liljas A. 2000. The end of the begining: structural studies of ribosomal proteins. Current Opinion in Structural Biology 10, 633-636.
13. Chen MH, Sheng J, Hind G, Handa AK, Citovsky V. 2000. Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO Journal 19, 913-920.
14. Collet H, Butowt R, Smith J, Farrant J, Illing N. 2003. Photosynthetic genes are differentially transcribed during the dehydration-rehydration cycle in the resuurection plant, Xerophyta humilis. Journal of Experimental Botany 54, 2593-2595.
15. Desikan R, A-H-Mackerness S, Hancock JT, Neill SJ. 2001. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiology 127, 159-172.
16. Domingo C, Sauri A, Mansilla E, Conejero V, Vera P. 1999. Identification of a novel peptide motif that mediates cross-linking of proteins to cell walls. The Plant Journal 20, 563-570.
17. Douce R, Bourguignon J, Neuburger M, Rebeille F. 2001. The glycine decarboxylase system: a fascinating complex. Trends in Plant Science 6, 167-176.
18. Douce R, Neuburger M. 1999. Biochemical dissection of photorespiration. Current Opinion in Plant Biology 2, 214-222.
19. Dresios J, Panopoulos P, Suzuki K, Synetos D. 2003. A dispensable yeast ribosomal protein optimizes peptidyltransferase activity and affects translocation. Journal of Biological Chemistry 278, 3314-3322.
20. Graciet E, Lebreton S, Gontero B. 2004. Emergence of new regulatory mechanisms in the Benson-Calvin pathway via protein-protein interactions: a glyceraldehyde-3-phosphate dehydrogenase/CP12/phosphoribulokinase complex. Journal of Experimental Botany 55, 1245-1254.
21. Hell R, Hillebrand H. 2001. Plant concepts for mineral acquisition and allocation. Current Opinion in Biotechnology 12, 161-168.
22. Herouart D, Van Montagu M, Inze D. 1993. Redox-activated expression of the cytosolic copper/zinc superoxide dismutase gene in Nicotiana. Proceedings of the National Academy of Sciences, USA 90, 3108-3112.
23. Herrin DL, Schmidt GW, 1988. Rapid, reversible staining of northern blots prior to hybridization. Biotechniques 6, 196-200.
24. Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K. 2003. 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. The Plant Journal 33, 651-663.
25. Ho CL, Saito K. 2001. Molecular biology of the plastidic phosphorylated serine biosynthetic pathway in Arabidopsis thaliana. Amino Acids 20, 243-259.
26. Houtz RL, Portis Jr AR. 2003. The life of ribulose 1,5-bisphosphate carboxylase/oxygenase: post-translational facts and mysteries. Archives of Biochemistry and Biophysics 414, 150-158.
27. Jensen PE, Gilpin M, Knoetzel J, Scheller HV. 2000. The PSI-K subunit of photosystem I is involved in the interaction between light-harvesting complex I and the photosystem I reaction center core. Journal of Biological Chemistry 275, 24701-24708.
28. Kandlbinder A, Finkemeier I, Wormuth D, Hanitzsch M, Dietz KJ. 2004. The antioxidant status of photosynthesizing leaves under nutrient deficiency: redox regulation, gene expression, and antioxidant activity in Arabidopsis thaliana. Physiologia Plantarum 120, 63-73.
29. Kawano T. 2003. Roles of the reactive oxygen species-generating peroxidase reactions in plant defence and growth induction. Plant Cell Reports 21, 829-837.
30. Kiss E, Huguet T, Poinsot V, Batut J. 2004. The typA gene is required for stress adaptation as well as for symbiosis of Sinorhizobium meliloti 1021 with certain Medicago truncatula lines. Molecular Plant-Microbe Interactions 17, 235-244.
31. Knörzer OC, Durner J, Böger P. 1996. Alterations in the antioxidative systems of suspension-cultured soybean cells (Glycine max) induced by oxidative stress. Physiologia Plantarum 97, 388-396.
32. Legg PD, Collins GB, Litton CC. 1970. Registration of LA Burley 21 tobacco germplasm. Crop Science 10, 212.
33. Linthorst HJ, Brederode FT, van der Does C, Bol JF. 1993. Tobacco proteinase inhibitor I genes are locally, but not systemically induced by stress. Plant Molecular Biology 21, 985-992.
34. Luo JH, Puc JA, Slosberg ED, Yao Y, Bruce JN, Wright Jr TC, Becich MJ, Parsons R. 1999. Differential subtraction chain, a method for identifying differences in genomic DNA and mRNA. Nucleic Acids Research 27, e24.
35. Mahalingam R, Gomez-Buitrago A, Eckardt N, Shah N, Guevara-Garcia A, Day P, Raina R, Fedoroff NV. 2003. Characterizing the stress/defence transcriptome of Arabidopsis. Genome Biology 4, R20.
36. Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK. 2002. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419, 399-403.
37. Maruyama A, Saito K, Ishizawa K. 2001. Beta-cyanoalanine synthase and cysteine synthase from potato: molecular cloning, biochemical characterization, and spatial and hormonal regulation. Plant Molecular Biology 46, 749-760.
38. Maruyama-Nakashita A, Inoue E, Watanabe-Takahashi A, Yamaya T, Takahashi H. 2003. Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiology 132, 597-605.
39. Meshi T, Taoka KI, Iwabuchi M. 2000. Regulation of hi stone gene expression during the cell cycle. Plant Molecular Biology 43, 643-657.
40. Migge A, Bork C, Hell R, Becker TW. 2000. Negative regulation of nitrate reductase gene expression by glutamine or asparagine accumulating in leaves of sulfur-deprived tobacco. Planta 211, 587-595.
41. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405-410.
42. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473-493.
43. Naeem HA, MacRitchie F. 2003. Effect of sulphur nutrition on agronomic and quality attributes of wheat. In: Abrol YP, Ahmad A, eds. Sulphur in plants. Dordrecht, The Netherlands: Kluwer Academic Publishers, 305-322.
44. Nakane E, Kawakita K, Doke N, Yoshioka H. 2003. Elicitation of primary and secondary metabolism during defence in the potato. Journal of General Plant Pathology 69, 378-384.
45. Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R. 2003. Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. The Plant Journal 33, 633-650.
46. Nikiforova V, Kempa S, Zeh M, Maimann S, Kreft O, Casazza AP, Riedel K, Tauberger E, Hoefgen R, Hesse H. 2002. Engineering of cysteine and methionine biosynthesis in potato. Amino Acids 22, 259-278.
47. Okamura M. 1980. An improved method for determination of L-ascorbic acid and L-dehydroascorbic acid in blood plasma. Clinica Chimica Acta 103, 259-268.
48. Orlandi I, Bettiga M, Alberghina L, Vai M. 2004. Transcriptional profiling of ubp10 null mutant reveals altered subtelomeric gene expression and insurgence of oxidative stress response. Journal of Biological Chemistry 279, 6414-64125.
49. Otto B, Kaldenhoff R. 2000. Cell-specific expression of the mercury-insensitive plasma-membrane aquaporin NtAQP1 from Nicotiana tabacum. Planta 211, 167-172.
50. Palma M, DeLuca D, Worgall S, Quadri LE. 2004. Transcriptome analysis of the response of Pseudomonas aeruginosa to hydrogen peroxide. Journal of Bacteriology 186, 248-252.
51. Petrucco S, Bolchi A, Foroni C, Percudani R, Rossi GL, Ottonello S. 1996. A maize gene encoding an NADPH binding enzyme highly homologous to isoflavone reductases is activated in response to sulfur starvation. The Plant Cell 8, 69-80.
52. Pfannschmidt T. 2003. Chloroplast redox signals: how photosynthesis controls its own genes. Trends in Plant Science 8, 33-41.
53. Pfannschmidt T, Schutze K, Fey V, Sherameti I, Oelmuller R. 2003. Chloroplast redox control of nuclear gene expression - a new class of plastid signals in interorganellar communication. Antioxidants and Redox Signalling 5, 95-101.
54. Rizhsky L, Liang H, Mittler R. 2002. The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiology 130, 1143-1151.
55. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
56. Scandalios JG. 2002. The rise of ROS. Trends in Biochemical Sciences 27, 483-486.
57. Schafer FQ, Buettner GR. 2001. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radicals in Biology and Medicine 30, 1191-1212.
58. Schuller C, Mamnun YM, Mollapour M, Krapf G, Schuster M, Bauer BE, Piper PW, Kuchler K. 2004. Global phenotypic analysis and transcriptional profiling defines the weak acid stress response regulon in Saccharomyces cerevisiae. Molecular Biology of the Cell 15, 706-720.
59. Scippa GS, Di Michele M, Onelli E, Patrignani G, Chiatante D, Bray EA. 2004. The histone-like protein H1-S and the response of tomato leaves to water deficit. Journal of Experimental Botany 55, 99-109.
60. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K. 2001. Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. The Plant Cell 13, 61-72.
61. Siefritz F, Tyree MT, Lovisolo C, Schubert A, Kaldenhoff R. 2002. PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. The Plant Cell 14, 869-876.
62. Simon-Plas F, Elmayan T, Blein JP. 2002. The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. The Plant Journal 31, 137-147.
63. Sirko A, Błaszczyk A, Liszewska F, Kazimierczuk K, Gaganidze D. 2003. Genetic engineering of oxidative stress resistance in plants. In: Abrol YP, Ahmad A, eds. Sulphur in plants. Dordrecht, The Netherlands: Kluwer Academic Publishers, 245-263.
64. Sousa MC, McKay DB. 2001. Structure of the universal stress protein of Haemophilus influenzae. Structure (Cambridge) 9, 1135-1141.
65. Sullivan JA, Shirasu K, Deng XW. 2003. The diverse roles of ubiquitin and the 26S proteasome in the life of plants. Nature Reviews Genetics 4, 948-958.
66. Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, Engler JA, Engler G, Van Montagu M, Saito K. 1997. Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 94, 11102-11107.
67. Takahashi Y, Nagata T. 1992. parB: an auxin-regulated gene encoding glutathione S-transferase. Proceedings of the National Academy of Sciences, USA 89, 56-59.
68. Takahashi Y, Sakai T, Ishida S, Nagata T. 1995. Identification of auxin-responsive elements of parB and their expression in apices of shoot and root. Proceedings of the National Academy of Sciences, USA 92, 6359-6563.
69. Takemoto D, Doke N, Kawakita K. 2001. Characterization of elicitor-inducible tobacco genes isolated by differential hybridization. Journal of General Plant Pathology 67, 89-96.
70. Ueda T, Seo S, Ohashi Y, Hashimoto J. 2000. Circadian and senescence-enhanced expression of a tobacco cysteine protease gene. Plant Molecular Biology 44, 649-657.
71. Vandenabeele S, Van Der Kelen K, Dat J, et al. 2003. A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proceedings of the National Academy of Sciences, USA 100, 16113-16118.
72. Varotto C, Pesaresi P, Jahns P, Lessnick A, Tizzano M, Schiavon F, Salamini F, Leister D. 2002. Single and double knockouts of the genes for photosystem I subunits G, K, and H of Arabidopsis. Effects on photosystem I composition, photosynthetic electron flow, and state transitions. Plant Physiology 129, 616-624.
73. Vercauteren I, de Almeida Engler J, De Groodt R, Gheysen G. 2002. An Arabidopsis thaliana pectin acetylesterase gene is up-regulated in nematode feeding sites induced by root-knot and cyst nematodes. Molecular Plant Microbe Interactions 15, 404-407.
74. Vierstra RD. 2003. The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends in Plant Science 8, 135-142.
75. Vincken JP, Schols HA, Oomen RJ, McCann MC, Ulvskov P, Voragen AG, Visser RG. 2003. If homogalacturonan were a side chain of rhamnogalacturonan. I. Implications for cell wall architecture. Plant Physiology 132, 1781-1789.
76. Wang KL, Li H, Ecker JR. 2002. Ethylene biosynthesis and signalling networks. The Plant Cell 14, S131-S151.
77. Wang R, Okamoto M, Xing X, Crawford NM. 2003. Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiology 132, 556-567.
78. Wu HM, Zou J, May B, Gu Q, Cheung AY. 1993. A tobacco gene family for flower cell wall proteins with a proline-rich domain and a cysteine-rich domain. Proceedings of the National Academy of Sciences, USA 90, 6829-6833.
79. Yang T, Poovaiah BW. 2002. Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proceedings of the National Academy of Sciences, USA 99, 4097-4102.
80. Yonekura-Sakakibara K, Ashikari T, Tanaka Y, Kusumi T, Hase T. 1998. Molecular characterization of tobacco sulfite reductase: enzyme purification, gene cloning, and gene expression analysis. Journal of Biochemistry (Tokyo) 124, 615-621.
81. Yoshida K, Kaothien P, Matsui T, Kawaoka A, Shinmyo A. 2003. Molecular biology and application of plant peroxidase genes. Applied Microbiology and Biotechnology 60, 665-670.
82. Youssefian S, Nakamura M, Orudgev E, Kondo N. 2001. Increased cysteine biosynthesis capacity of transgenic tobacco overexpressing an O-acetylserine(thiol) lyase modifies plant responses to oxidative stress. Plant Physiology 126, 1001-1011.