Nodule-enhanced expression of a sucrose phosphate synthase gene member (MsSPSA) has a role in carbon and nitrogen metabolism in the nodules of alfalfa (Medicago sativa L.)

Planta

Volumn 231, Issue 2, 2010, Pages 233-244

  Aleman, Lorenzo ^a   Ortega, Jose Luis ^a   Martinez Grimes, Martha ^a   Seger, Mark ^a   Holguin, Francisco Omar ^a   Uribe, Diana J ^a   Garcia Ibilcieta, David ^a   Sengupta Gopalan, Champa ^a  

^a NEW MEXICO STATE UNIVERSITY   (United States)

Author keywords

Carbon metabolism; Medicago sativa; Nitrogen metabolism; Sucrose phosphate synthase; Sucrose synthesis; Symbiotic nodules

Indexed keywords

CARBON; GLUCOSYLTRANSFERASE; MESSENGER RNA; NITROGEN; STARCH; SUCROSE PHOSPHATE SYNTHASE; SUCROSE-PHOSPHATE SYNTHASE; VEGETABLE PROTEIN;

ALFALFA; ALLOSTERISM; ARTICLE; CARBOHYDRATE METABOLISM; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; ION EXCHANGE CHROMATOGRAPHY; METABOLISM; MICROBIOLOGY; MULTIGENE FAMILY; NITROGEN FIXATION; NODULATION; PHYSIOLOGY; PLANT GENE; PLANT LEAF; SINORHIZOBIUM MELILOTI; SOLUBILITY; SYMBIOSIS; WESTERN BLOTTING;

ALLOSTERIC REGULATION; BLOTTING, WESTERN; CARBOHYDRATE METABOLISM; CARBON; CHROMATOGRAPHY, ION EXCHANGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLUCOSYLTRANSFERASES; MEDICAGO SATIVA; MULTIGENE FAMILY; NITROGEN; NITROGEN FIXATION; PLANT LEAVES; PLANT PROTEINS; RNA, MESSENGER; ROOT NODULES, PLANT; SINORHIZOBIUM MELILOTI; SOLUBILITY; STARCH; SYMBIOSIS;

MEDICAGO SATIVA; SINORHIZOBIUM MELILOTI;

EID: 77949773450     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-009-1043-y     Document Type: Article

References (51)

1. Baier MC, Barsch A, Kuster H, Hohnjec N (2007) Antisense repression of the Medicago truncatula nodule-enhanced sucrose synthase leads to a handicapped nitrogen fixation mirrored by specific alterations in the symbiotic transcriptome and metabolome. Plant Physiol 145: 1600-1618.
2. Barratt DHP, Barber L, Kruger NJ, Smith AM, Wang TL, Martin C (2001) Multiple, distinct isoforms of sucrose synthase in pea. Plant Physiol 127: 655-664.
3. Barsch A, Tellstrom V, Patschkowski T, Kuster H, Niehaus K (2006) Metabolite profiles of nodulated alfalfa plants indicate that distinct stages of nodule organogenesis are accompanied by global physiological adaptations. Mol Plant-Microbe Interact 19: 998-1013.
4. Baxter CJ, Foyer CH, Turner J, Rolfe SA, Quik WP (2003) Elevated sucrose-phosphate synthase activity in transgenic tobacco sustains photosynthesis in older leaves and alters development. J Exp Bot 54: 1813-1820.
5. Castleden CK, Aoki N, Gillespie VJ, MacRae EA, Quik WP, Buchner P, Foyer CH, Furbank RT, Lunn JE (2004) Evolution and function of the sucrose phosphate synthase gene families in wheat and other grasses. Plant Physiol 135: 1-12.
6. Chen S, Hajirezaei M, Börnke F (2005) Differential expression of sucrose-phosphate synthase isoenzymes in tobacco reflects their functional specialization during dark governed starch mobilization in source leaves. Plant Physiol 139: 1163-1174.
7. Choi HK, Kim D, Uhm T, Limpens E, Lim H, Mun JH, Kalo P, Penmetsa RV, Seres A, Kulikova O, Roe BA, Bisseling T, Kiss GB, Cook DR (2004) A sequence-based genetic map of Medicago truncatula and comparison of marker colinearity with M. sativa. Genetics 166: 1463-1502.
8. Colebatch G, Kloska S, Trevaskis B, Freund S, Altmann T, Udvardi MK (2002) Novel aspects of symbiotic nitrogen fixation uncovered by transcript profiling with cDNA arrays. Mol Plant-Microbe Interact 15: 411-420.
9. Cumino AC, Marcozzi C, Barreiro R, Salerno GL (2007) Carbon cycling in Anabaena sp. PCC 7120. Sucrose synthesis in the heterocysts and possible role in nitrogen fixation. Plant Physiol 143: 1385-1397.
10. De Vries SC, Springer J, Wessels JGH (1982) Diversity of abundant mRNA sequences and patterns of protein synthesis in etiolated and greened pea seedlings. Planta 156: 120-135.
11. Flemetakis E, Dimou M, Cotzur D, Efrose RC, Alvalakis G, Colebatch G, Udvardi MK, Katinakis P (2003) A sucrose transporter, LjSUT4, is up-regulated during Lotus japonicus nodule development. J Exp Bot 54: 1789-1791.
12. Flemetakis E, Efrose RC, Ott T, Stedel C, Alvalakis G, Udvardi MK, Katinakis P (2006) Spatial and temporal organization of sucrose metabolism in Lotus japonicus nitrogen-fixing nodules suggests a role for the elusive alkaline/neutral invertase. Plant Mol Biol 62: 53-69.
13. Fung RWM, Langenkamper G, Gardner RC, MacRae E (2003) Differential expression within an SPS gene family. Plant Sci 164: 459-470.
14. Geigenberger P, Stitt M (1991) A futile cycle of sucrose synthesis and degradation is involved in regulating partitioning between sucrose, starch and respiration in cotyledons of germinating Ricinus communis L. seedlings when phloem transport is inhibited. Planta 185: 81-90.
15. Geigenberger P, Reimholz R, Geiger M, Merlo L, Canale V, Stitt M (1997) Regulation of sucrose and starch metabolism in potato tubers in response to short-term water deficit. Planta 201: 502-518.
16. Gordon AJ, Minchin FR, James CL, Komina O (1999) Sucrose synthase in legume nodules is essential for nitrogen fixation. Plant Physiol 120: 867-878.
17. Graham PH, Vance CP (2003) Legumes: importance and constrains to greater use. Plant Physiol 131: 872-877.
18. Grof CPL, So CTE, Perroux JM, Bonnett GD, Forrester RI (2006) The five families of sucrose-phosphate synthase genes in Saccharum spp. are differentially expressed in leaves and stem. Funct Plant Biol 33: 605-610.
19. Harlow E, Lane D (1998) Antibodies, a laboratory manual. Cold Spring Harbor Laboratory Press, New York.
20. Hirsch AM, Bang M, Ausubel FM (1983) Ultrastructural analysis of ineffective alfalfa nodules formed by nif: Tn5 mutants of Rhizobium meliloti. J Bacteriol 155: 367-380.
21. Hohnjec N, Perlick AM, Pühler A, Küster H (2003) The Medicago truncatula sucrose synthase gene MtSucS1 is activated both in the infected region of root nodules and in the cortex of roots colonized by arbuscular mycorrhizal fungi. Mol Plant-Microbe Interact 16: 903-915.
22. Horst I, Welham T, Kelly S, Kaneko T, Sato S, Tabata S, Parniske M, Wang TL (2007) TILLING mutants of Lotus japonicus reveal that nitrogen assimilation and fixation can occur in the absence of nodule-enhanced sucrose synthase. Plant Physiol 144: 806-820.
23. Hubbard NL, Pharr DM, Huber SC (1991) Sucrose phosphate synthase and other sucrose metabolizing enzymes in fruits of various species. Physiol Plant 82: 191-196.
24. Huber SC (2007) Exploring the role of protein phosphorylation in plants: from signalling to metabolism. Biochem Soc Trans 35: 28-32.
25. Huber SC, Huber JL (1996) Role and regulation of sucrose-phosphate synthase in higher plants. Annu Rev Plant Physiol Plant Mol Biol 47: 431-444.
26. Im KH (2004) Expression of sucrose-phosphate synthase (SPS) in non-photosynthetic tissues of maize. Mol Cells 17: 404-409.
27. Ingram J, Chandler JW, Gallagher L, Salamini F, Bartels D (1997) Analysis of cDNA clones encoding sucrose-phosphate synthase in relation to sugar interconversions associated with dehydration in the resurrection plant Craterostigma plantagineum Hochst. Plant Physiol 115: 113-121.
28. Komatsu A, Takanokura Y, Omura M, Akihama T (1996) Cloning and molecular analysis of cDNAs encoding three sucrose phosphate synthase isoforms from a citrus fruit (Citrus unshiu Marc). Mol Gen Genet 252: 346-351.
29. Langenkamper G, Fung RWK, Newcomb RD, Atkinson RG, Gardner RC, MacRae EA (2002) Sucrose phosphate synthase genes in plants belong to three different families. J Mol Evol 54: 322-332.
30. Li CR, Zhang XB, Hew CS (2003) Cloning of a sucrose-phosphate synthase gene highly expressed in flowers from the tropical epiphytic orchid Oncidium goldiana. J Exp Bot 54: 2189-2191.
31. Lodwig EM, Hosie AHF, Bourdes A, Findlay K, Allaway D, Karunakaran R, Downie JA, Poole PS (2003) Amino acid recycling drives nitrogen fixation in the legume-rhizobium symbiosis. Nature 422: 722-726.
32. Loreti E, Bellis LD, Alpi A, Perata P (2001) Why and how do plants sense sugars? Ann Bot 88: 803-812.
33. Lunn JE, MacRae EA (2003) New complexities in the synthesis of sucrose. Curr Opinion Plant Biol 6: 208-214.
34. F-phosphate phosphohydrolase from plants. Proc Natl Acad Sci USA 97: 12914-12919.
35. Lutfiyya LL, Xu N, D'Ordine RL, Morrell JA, Miller PW, Duff SMG (2007) Phylogenetic and expression analysis of sucrose phosphate synthase isozymes in plants. J Plant Physiol 164: 923-933.
36. Nguyen-Quoc B, Foyer CH (2001) A role for 'futile cycles' involving invertase and sucrose synthase in sucrose metabolism of tomato fruit. J Exp Bot 52: 881-889.
37. 1) affects transcript stability and protein accumulation in transgenic alfalfa. Plant J 45: 832-846.
38. Rae AL, Grof CPL, Casu RE, Bonnett GD (2005) Sucrose accumulation in the sugarcane stem: pathway and control points for transport and compartmentation. Field Crop Res 92: 159-168.
39. Reich PB, Hungate BA, Luo Y (2006) Carbon-nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Annu Rev Ecol Evol Syst 37: 611-636.
40. Reimholtz R, Geiger M, Haake V, Deiting U, Krause KP, Sonnewald U, Stitt M (1997) Potato plants contain multiple forms of sucrose phosphate synthase, which differ in their tissue distribution, their levels during development, and their response to low temperature. Plant Cell Environ 20: 291-305.
41. Roby C, Cortes S, Gromova M, Le Bail JL, Roberts JK (2002) Sucrose cycling in heterotrophic plant cell metabolism: first step towards an experimental model. Mol Biol Rep 29: 145-149.
42. Tesfaye M, Samac DA, Vance CP (2006) Insights into symbiotic nitrogen fixation in Medicago truncatula. Mol Plant-Microbe Interact 19: 330-341.
43. Toroser D, Huber SC (1997) Protein phosphorylation as a mechanism for osmotic stress activation of sucrose-phosphate synthase in spinach leaves. Plant Physiol 114: 947-955.
44. Trevanion SJ, Castleden CK, Foyer CH, Furbank RT, Quick WP, Lunn JE (2004) Regulation of sucrose-phosphate synthase in wheat (Triticum aestivum) leaves. Funct Plant Biol 31: 685-695.
45. Trevaskis B, Colebatch G, Desbrosses G, Wandrey M, Wienkoop S, Saalbach G, Udvardi M (2002) Differentiation of plant cells during symbiotic nitrogen fixation. Comp Funct Genom 3: 151-157.
46. Wacek TJ, Alm D (1978) Easy to make 'Leonard jar'. Crop Sci 18: 514-515.
47. Welham T, Pike J, Horst I, Flemetakis E, Katinakis P, Kaneko T, Sato S, Tabata S, Perry J, Parniske M, Wang TL (2009) A cytosolic invertase is required for normal growth and cell development in the model legume, Lotus japonicus. J Exp Bot 60: 3353-3365.
48. Wienkoop S, Larrainzar E, Glinski M, González EM, Arrese-Igor C, Weckwerth W (2008) Absolute quantification of Medicago truncatula sucrose synthase isoforms and N-metabolism enzymes in symbiotic root nodules and the detection of novel nodule phosphoproteins by mass spectrometry. J Exp Bot 59: 3307-3315.
49. Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. CRC Crit Rev Plant Sci 19: 31-67.
50. Xu Y, Li HB, Zhu YX (2007) Molecular biological and biochemical studies reveal new pathways important for cotton fiber development. J Int Plant Biol 49: 69-74.
51. Zuk M, Weber R, Szopa J (2005) 14-3-3 Protein down-regulates key enzyme activities of nitrate and carbohydrate metabolism in potato plants. J Agric Food Chem 53: 3454-3460.