Genomic organization and expression properties of the MtSucS1 gene, which encodes a nodule-enhanced sucrose synthase in the model legume Medicago truncatula

Molecular and General Genetics

Volumn 261, Issue 3, 1999, Pages 514-522

  Hohnjec, N ^a   Becker, J D ^a   Puhler A ^a   Perlick, A M ^a   Kuster H ^a  

^a BIELEFELD UNIVERSITY   (Germany)

Author keywords

Medicago trunctula; Nodule carbon motabolism; Sink organ; Symbiotic nitrogen fixation

Indexed keywords

COMPLEMENTARY DNA; MESSENGER RNA; PLANT DNA; SUCROSE; SYNTHETASE;

AMINO ACID SEQUENCE; ARTICLE; BEAN; DNA SEQUENCE; EXON; GENE EXPRESSION; GENE ISOLATION; GENE STRUCTURE; LEGUME; MOLECULAR WEIGHT; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PEA; PLANT ROOT; PRIORITY JOURNAL; PROMOTER REGION; SEQUENCE HOMOLOGY; SOUTHERN BLOTTING; START CODON;

AMINO ACID SEQUENCE; BASE SEQUENCE; CHROMOSOME MAPPING; DNA, COMPLEMENTARY; DNA, PLANT; EXONS; GENE EXPRESSION; GENES, PLANT; GENES, REGULATOR; GENOME, PLANT; GLUCOSYLTRANSFERASES; MEDICAGO SATIVA; MOLECULAR SEQUENCE DATA; PLANT ROOTS; PROMOTER REGIONS (GENETICS); SEQUENCE HOMOLOGY, AMINO ACID;

EMBRYOPHYTA; MEDICAGO; MEDICAGO TRUNCATULA; PHASEOLUS (ANGIOSPERM); PISUM SATIVUM; VICIA FABA;

EID: 0032967839     PISSN: 00268925     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004380050995     Document Type: Article

References (87)

1. Akazawa T, Okamoto K (1980) Biosynthesis and metabolism of sucrose. Biochem Plants 3:199-220
2. Anthon GE, Emmerich DW (1990) Developmental regulation of enzymes of sucrose and hexose metabolism in effective and ineffective soybean nodules. Plant Physiol 92:346-351
3. Arai M, Mori H, Imazeki H (1992) Expression of the gene for sucrose synthase during growth of mung bean seedlings. Plant Cell Physiol 33:503-506
4. Arnold W, Pühler A (1988) A family of high-copy-number plasmid vectors with single end-label sites for rapid nucleotide sequencing. Gene 70:171-179
5. Avigad G (1982) Sucrose and other disaccarides. In: Loewus FA, Tanner W (eds) Encyclopedia of Plant Physiology (New Series), vol 13A. Springer, Berlin pp 216-347
6. Barker DG, Bianchi S, Blondon F, Dattée Y, Duc G, Essad S, Flament P, Gallusci P, Génier G, Guy P, Muel X, Tourneur J, Dénarié J, Huguet T (1990) Medicago truncatula, a model plant for studying the molecular genetics of the Rhizobium-legume symbiosis. Plant Mol Biol Rep 8:40-49
7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
8. Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50:349-383
9. Brewin NJ (1991) Development of the legume root nodule. Annu Rev Cell Biol 7:191-226
10. Buchner P, Poret M, Rochat C (1998) Cloning and characterization of a cDNA (Accession No. AJ001071) encoding a second sucrose synthase gene in pea (Pisum sativum L.). Plant Physiol 117:719
11. Bullock WC, Fernandez JM, Short JM (1987) XL1Blue: a high efficiency plasmid transforming recA Escherichia coli strain with beta-galactosidase selection. BioTechniques 5:376-379
12. Callis J, Fromm M, Walbot V (1987) Introns increase gene expression in cultured maize cells. Genes Dev 1:1183-1200
13. Chopra S, Del-Favero J, Dolferus R, Jacobs M (1992) Sucrose synthase of Arabidopsis: genomic cloning and sequence characterization. Plant Mol Biol 18:131-134
14. Coba de la Pena T, Frugier F, McKhann HI, Bauer P, Brown S, Kondorosi A, Crespi M (1997) A carbonic anhydrase gene is induced in the nodule primordium and its cell-specific expression is controlled by the presence of Rhizobium during development. Plant J 11:407-420
15. Cohn J, Day BR, Stacey G (1998) Legume nodule organogenesis. Trends Plant Sci 3:105-110
16. Covitz PA, Smith LS, Long SR (1998) Expressed sequence tags from a root-hair-enriched Medicago truncatula cDNA library. Plant Physiol 117:1325-1332
17. De Bruijn FJ, Chen R, Fujimoto SY, Pinaev A, Silver D, Szczyglowski K (1994) Regulation of nodulin gene expression. Plant Soil 161:59-68
18. Déjardin A, Rochat C, Maugenest S, Boutin JP (1997) Purification, characterization and physiological role of sucrose synthase in the pea seed coat (Pisum sativum L.). Planta 201:128-137
19. Delauney AJ, Verma DPS (1988) Cloned nodulin genes for symbiotic nitrogen fixation. Plant Mol Biol Rep 6:279-285
20. Diaz I, Royo J, O'Connor A, Carbonero P (1995) The promoter of the gene Itr1 from barley confers a different tissue specificity in transgenic tobacco. Mol Gen Genet 248:592-598
21. Forde BG, Freeman J, Oliver JE, Pineda M (1990) Nuclear factors interact with conserved A/T-rich elements upstream of a nodule-enhanced glutamine synthetase gene from french bean. Plant Cell 2:925-939
22. Franssen HJ, Yiyn I, Yang WC, Bisseling T (1992) Developmental aspects of the Rhizobium-legume symbiosis. Plant Mol Biol 19:89-107
23. Frischauf AM, Lehrach H, Poustka A, Murray N (1983) Lambda replacement vectors carrying polylinker sequences. J Mol Biol 170:827-842
24. Fu M, Park WD (1995) Sink-and vascular-associated sucrose synthase functions are encoded by different gene classes in potato. Plant Cell 7:1369-1385
25. Gamas P, Niebel F de C, Lescure N, Cullimore J (1996) Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development. Mol Plant-Microbe Interact 9:233-242
26. Gordon AJ, Thomas BJ, Reynolds PHS (1992) Localization of sucrose synthase in soybean root nodules. New Phytol 122:35-44
27. Gordon AJ, Skøt L, Webb KJ, Minchin FR, James CL (1998) Down regulation of nodule sucrose synthase by mutation and antisense. In: Elmerich C, Kondorosi A, Newton WE (eds) Biological nitrogen fixation for the 21st century. Kluwer Academic Publishers, Dordrecht, p 473
28. Hawker JS (1985) Sucrose. In: Dey PM, Dixon RA (eds) Biochemistry of storage carbohydrates in green plants. Academic Press, London, pp 1-51
29. Heim U, Weber H, Bäumlein H, Wobus U (1993) A sucrose-synthase gene of Vicia faba L.: expression pattern in developing seeds in relation to starch synthesis and metabolic regulation. Planta 191:394-401
30. Henikoff S (1984) Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28:351-359
31. Huber SC, Huber JL, Liao PC, Gage DA, McMichael RW Jr, Chourey PS, Hannah LC, Koch K (1996) Phosphorylation of serine-15 of maize leaf sucrose synthase. Occurrence in vivo and possible regulatory significance. Plant Physiol 112:793-802
32. Joshi CP (1987a) An inspection of the domain between putative TATA box and translation start site in 79 plant genes. Nucleic Acids Res 15:6643-6653
33. Joshi CP (1987b) Putative polyadenylation signals in nuclear genes of higher plants: a compilation and analysis. Nucleic Acids Res 15:9627-9640
34. Joshi CP, Zhou H, Huang X, Chiang VL (1997) Context sequences of translation initiation in plants. Plant Mol Biol 35:993-1001
35. Khyse-Andersen J (1984) Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J Biochem Biophys Methods 10:203-209
36. Kishimoto A, Nishimaya K, Nakanishi H, Uratsuji Y, Nomura H, Takeyama Y, Nishizuka Y (1985) Studies on the phosphorylation of myelin basic protein by protein kinase C and adenosine 3′:5′-monophosphate-dependent protein kinase. J Biol Chem 260:12492-12499
37. Koch KE, Nolte KD, Duke ER, McCarthy DR, Avigne WT (1992) Sugar levels modulate differential expression of maize sucrose synthase genes. Plant Cell 4:59-69
38. Kouchi H, Katsuhiko F, Katagiri H, Minamisawa K, Tajima S (1988) Isolation and enzymylogical characterization of infected and uninfected cell protoplasts from root nodules of Glycine max. Physiol Plant 73:327-334
39. Küster H, Frühling M, Perlick AM, Pühler A (1993) The sucrose synthase gene is predominantly expressed in the root nodule tissue of Vicia faba. Mol Plant-Microbe Interact 6:507-514
40. Küster H, Quandt H-J, Broer I, Perlick AM, Pühler A (1995a) The promoter of the Vicia faba L. VfENOD-GRP3 gene encoding a glycine-rich early nodulin mediates a predominant gene expression in the interzone II-III region of transgenic Vicia hirsuta root nodules. Plant Mol Biol 29:759-772
41. Küster H, Schröder G, Frühling M, Pich U, Rieping M, Schubert I, Perlick AM, Pühler A (1995b) The nodule-specific VfENOD-GRP3 gene encoding a glycine-rich early nodulin is located on chromosome I of Vicia faba L. and is predominantly expressed in the interzone II-III of root nodules. Plant Mol Biol 28:405-421
42. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
43. Laursen NB, Larsen K, Knudsen JY, Hoffmann HJ, Poulsen C, Marcker KA, Jensen EØ (1994) A protein binding AT-rich sequence in the soybean leghemoglobin c3 promoter is a general cis element that requires proximal DNA elements to stimulate transcription. Plant Cell 6:659-668
44. Lindblom S, Ek P, Muszynska G, Ek B, Szczegielniak J, Engstrom L (1997) Phosphorylation of sucrose synthase from maize seedlings. Acta Biochem Pol 44:809-817
45. Maas C, Laufs J, Grant S, Korfhage C, Werr W (1991) The combination of a novel stimulatory element in the first exon of the maize Shrunken-1 gene with the following intron 1 enhances reporter gene expression up to 1000-fold. Plant Mol Biol 16:199-207
46. Marana C, Garcia-Olmedo F, Carbonero P (1988) Linked sucrose synthase genes in group-7 chromosomes in hexaploid wheat (Triticum aestivum L.). Gene 63:253-260
47. Martin T, Frommer WB, Salanoubat M, Willmitzer L (1993) Expression of an Arabidopsis sucrose synthase gene indicates a role in metabolization of sucrose both during phloem loading and in sink organs. Plant J 4:367-377
48. McCarthy DR, Shaw JR, Hannah LC (1986) The cloning, genetic mapping and expression of the constitutive sucrose synthase locus of maize. Proc Natl Acad Sci USA 83:9099-9103
49. McElroy D, Zhang W, Cao J, Wu R (1990) Isolation of an efficient actin promoter for use in rice transformation. Plant Cell 2:163-171
50. Metz BA, Welters P, Hoffmann HJ, Jensen EØ, Schell J, de Bruijn FJ (1988) Primary structure and promoter analysis of leghemoglobin genes of the stem-nodulated tropical legume Sesbania rostrata: conserved coding sequences, cis-elements and transacting factors. Mol Gen Genet 214:181-191
51. Morell M, Copeland L (1984) Enzymes of sucrose breakdown in soybean nodules. Alkaline invertase. Plant Physiol 74:149-154
52. Morell M, Copeland L (1985) Sucrose synthase of soybean nodules. Plant Physiol 78:149-154
53. Mylona P, Pawlowski K, Bisseling T (1995) Symbiotic nitrogen fixation. Plant Cell 7:869-885
54. Oard JH, Paige DF, Simmonds JA, Gradziel TM (1990) Transient gene expression in maize, rice and wheat cells using an airgun apparatus. Plant Physiol 92:334ff
55. Pawlowski K (1997) Nodule-specific gene expression. Physiol Plantarum 99:617-631
56. Perlick AM, Pühler A (1993) A survey of transcripts expressed specifically in root nodules of broadbean (Vicia faba L.). Plant Mol Biol 22:957-970
57. Pridmore RD (1987) New and versatile cloning vectors with kanamycin-resistance marker. Gene 56:309-312
58. Proudfoot N (1991) Poly (A) signals. Cell 64:671-674
59. Ramlov KB, Laursen NB, Stougaard J, Marcker KA (1993) Site-directed mutagenesis of the organ-specific element in the soybean leghemoglobin lbc3 gene promoter. Plant J 4:577-580
60. Rothnie HM (1996) Plant mRNA 3′-end formation. Plant Mol Biol 32:43-61
61. Ross HA, Davies HV (1992) Purification and characterisation of sucrose synthase from the cotyledons of Vicia faba L. Plant Physiol 100:1008-1013
62. Salanoubat M, Belliard G (1987) Molecular cloning and sequencing of sucrose synthase cDNA from potato (Solanum tuberosum): preliminary characterization of sucrose synthase mRNA distribution. Gene 60:47-56
63. Salanoubat M, Belliard G (1989) The steady-state level of potato sucrose synthase mRNA is dependent on wounding, anaerobiosis and sucrose concentration. Gene 84:181-185
64. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual (2nd edn). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
65. Schuller KA, Werner D (1993) Phosphorylation of soybean (Glycine max L.) nodule phosphoenolpyruvate carboxylase in vitro decreases sensitivity to inhibition by L-malate. Plant Physiol 101:1267-1273
66. Shapiro MB, Senapathy P (1987) RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res 15:7155-7174
67. Sharypova LA, Onishchuk OP, Chesnokova ON, Fomina-Eshchenko JG, Simarov BV (1994) Isolation and characterization of Rhizobium meliloti Tn5 mutants showing enhanced symbiotic effectiveness. Microbiology 140:463-470
68. Skøt L, Minchin FR, Timms E, Fortune MT, Webb KJ, Gordon AJ (1996) Analysis of the two nodulins, sucrose synthase and ENOD2, in transgenic Lotus plants. Plant Soil 186:99-106
69. Skøt L, Gordon AJ, Timms E, James CE, Webb KJ, Mizen S (1997) Down-regulation of sucrose synthase expression and activity in transgenic hairy roots of Lotus japonicus. Symbiosis 22:241-254
70. Staden R (1986) The current status and portability of our sequence handling software. Nucleic Acids Res 14:217-231
71. Stougaard J, Sandal NN, Groen A, Kühle A, Marcker KA (1987) 5′ analysis of the soybean leghemoglobin lbc3 gene: regulatory elements required for promoter activity and organ specificity. EMBO J 6:3565-3569
72. Stougaard J, Jørgensen JE, Christensen T, Kühle A, Marcker KA (1990) Interdependence and nodule specificity of cis acting regulatory elements in the soybean leghemoglobin lbc3 and N23 gene promoters. Mol Gen Genet 220:353-360
73. Szczyglowski K, Szabados L, Fujimoto SY, Silver D, de Bruijn FJ (1994) Site-specific mutagenesis of the nodule-infected cell expression (NICE) element and the AT-rich element ATRE-BS2* of the Sesbania rostrata leghemoglobin glb3 promoter. Plant Cell 6:317-332
74. Thummler F, Verma DPS (1987) Nodulin-100 of soybean is the subunit of sucrose synthase regulated by the availability of free heme in nodules. J Biol Chem 262:14730-14736
75. Van Ghelue M, Ribeiro A, Solheim B, Akkermans ADL, Bisseling T, Pawlowski K (1996) Sucrose synthase and enolase expression in actinorhizal nodules of Alnus glutinosa: comparison with legume nodules. Mol Gen Genet 250:437-446
76. 2 fixation. In: Eimerich C, Kondorosi A, Newton WE (eds) Biological nitrogen fixation for the 21st century. Kluwer, Dordrecht, pp 443-448
77. Vasil V, Clancy M, Ferl RJ, Vasil IK, Hannah C (1990) Increased gene expression by the first intron of maize Shrunken-1 locus in grass species. Plant Physiol 91:1575-1579
78. Verma DPS, Hu C-A, Zhang M (1992) Root nodule development: origin, function and regulation of nodulin genes. Physiol Plant 85:253-265
79. Wang MB, Boulter D, Gatehouse JA (1992) A complete sequence of the rice sucrose synthase-1 (RSs1) gene. Plant Mol Biol 19:881-885
80. Wang TL, Hedley CL (1993) Seed mutants in Pisum. Pisum Genet 25:64-70
81. Weaver CD, Roberts DM (1992) Determination of the site of phosphorylation of nodulin 26 by the calcium-dependent protein kinase from soybean nodules. Biochemistry 31:8954-8959
82. Werr W, Frommer WB, Maas C, Starlinger P (1985) Structure of the sucrose synthase gene on chromosome 9 of Zea mays L. EMBO J 4:1373-1380
83. Xue Z, Larsen K, Jochimsen BU (1991) Oxygen regulation of uricase and sucrose synthase synthesis in soybean callus tissue is exerted at the mRNA level. Plant Mol Biol 16:899-906
84. Yu W-R, Wang A-Y, Juang R-H, Sung H-Y, Su J-C (1992) Isolation and sequence of rice sucrose synthase cDNA and genomic DNA. Plant Mol Biol 18:139-142
85. Zeng Y, Wu Y, Avigne WT, Koch KE (1998) Differential regulation of sugar-sensitive sucrose synthases by hypoxia and anoxia indicate complementary transcriptional and posttranscriptional responses. Plant Physiol 116:1573-1583
86. 2+-dependent protein kinase. FEBS Lett 410:126-130
87. Zhang XQ, Verma DPS, Paul S, Arredondo-Peter R, Miao GH, Kuismanen R, Klucas R, Chollet R (1997) Cloning of a full-length sucrose synthase cDNA from soybean (Glycine max) root nodules (Accession No. AF030231). Plant Physiol 115:1729