Plasmodesmata distribution and sugar partitioning in nitrogen-fixing root nodules of Datisca glomerata

Planta

Volumn 233, Issue 1, 2011, Pages 139-152

  Schubert, Maria ^a   Koteyeva, Nouria K ^b   Wabnitz, Philipp W ^a   Santos, Patricia ^c   Büttner, Michael ^d   Sauer, Norbert ^d   Demchenko, Kirill ^b,e   Pawlowski, Katharina ^a,c  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b KOMAROV BOTANICAL INSTITUTE   (Russian Federation)

^c STOCKHOLM UNIVERSITY   (Sweden)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^e ALL RUSSIA RESEARCH INSTITUTE FOR AGRICULTURAL MICROBIOLOGY   (Russian Federation)

Author keywords

Actinorhiza; Frankia; Invertase; Rutinose; Sucrose synthase; Sugar transport

Indexed keywords

BACTERIA (MICROORGANISMS); DATISCA GLOMERATA; FRANKIA;

EID: 78650728007     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-010-1285-8     Document Type: Article

References (70)

1. Abd-Alla MH, Koyro H-W, Schubert S, Peiter E (2000) Functional structure of the indeterminate Vicia faba L. root nodules: implications for metabolite transport. J Plant Physiol 157: 335-343.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
3. 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.
4. Benson DR, Silvester WB (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 57: 293-319.
5. Berg RH, Langenstein B, Silvester WB (1999) Development in the Datisca-Coriaria nodule type. Can J Bot 77: 1334-1350.
6. Berry AM, Murphy TM, Okubara PA, Jacobsen KR, Swensen SM, Pawlowski K (2004) Novel expression pattern of cytosolic glutamine synthetase in nitrogen-fixing root nodules of the actinorhizal host, Datiscaglomerata. Plant Physiol 135: 1849-1862.
7. +/hexose cotransporter (STP1) from Arabidopsis thaliana expressed in Xenopus oocytes. J Biol Chem 269: 20417-20424.
8. Bradford MM (1976) A rapid and sensitive method for the determination of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
9. Brewin NJ (2004) Plant cell wall remodelling in the rhizobium-legume symbiosis. Crit Rev Plant Sci 23: 293-316.
10. Büttner M, Sauer N (2000) Monosaccharide transporters in plants: structure, function and physiology. Biochim Biophys Acta 1465: 263-274.
11. Caspari T, Robl I, Stotz J, Tanner W (1996) Purification of the Chlorella HUP1 hexose-proton symporter to homogeneity and its reconstitution in vitro. Plant J 10: 1045-1053.
12. 14C-photoassimilates in soybean plants assimilating of symbiotic and nitrate nitrogen. Russ J Plant Physiol 45: 203-208.
13. Chung HJ, Sehnke PC, Ferl RJ (1999) The 14-3-3 proteins: cellular regulators of plant metabolism. Trends Plant Sci 4: 367-371.
14. Clawson ML, Bourret A, Benson DR (2004) Assessing the phylogeny of Frankia-actinorhizal plant nitrogen-fixing root nodule symbioses with Frankia 16S rRNA and glutamine synthetase gene sequences. Mol Phylogenet Evol 31: 131-138.
15. Complainville A, Brocard L, Roberts I, Dax E, Sever N, Sauer N, Kondorosi A, Wolf S, Oparka K, Crespi M (2003) Nodule initiation involves the creation of a new symplasmic field in specific root cells of Medicago species. Plant Cell 15: 2778-2791.
16. + transporters are expressed in roots of etiolated Glycine max seedlings. Plant Sci 169: 798-804.
17. Geigenberger P (2003) Regulation of sucrose to starch conversion in growing potato tubers. J Exp Bot 54: 457-465.
18. Gordon AJ, Minchin FR, James CL, Komina O (1999) Sucrose synthase in legume nodules is essential for nitrogen fixation. Plant Physiol 120: 867-877.
19. Guttenberger M (2000) Arbuscules of vesicular-arbuscular mycorrhizal fungi inhabit an acidic compartment within plant roots. Planta 211: 299-304.
20. Haigler CH, Ivanova-Datcheva M, Hogan PS, Salnikov VV, Hwang S, Martin K, Delmer DP (2001) Carbon partitioning to cellulose synthesis. Plant Mol Biol 47: 29-51.
21. Harrison MJ (1996) A sugar transporter from Medicago truncatula: altered expression pattern in roots during vesicular-arbuscular (VA) mycorrhizal associations. Plant J 9: 491-503.
22. Hoagland DR, Arnon DT (1938) The water-culture method for growing plants without soil. California Agriculture Experimental Station Circular, p 347.
23. Hohnjec N, Becker JD, Pühler A, Perlick AM, Küster H (1999) Genomic organization and expression properties of the MtSucS1 gene, which encodes a nodule-enhanced sucrose synthase in the model legume Medicago truncatula. Mol Gen Genet 261: 514-522.
24. Huber SC, Huber JL, Liao PC, Gage DA, McMichael P Jr, Courey PS, Hannah LC, Koch K (1996) Phosphorylation of serine-15 of maize leaf sucrose synthase. Plant Physiol 112: 793-802.
25. Jackson D (1991) In situ hybridization in plants. In Bowles DJ, Gurr SF, McPherson M (eds) Molecular plant pathology: a practical approach. Oxford University Press, Oxford, pp 163-174.
26. Jeong J, Suh S, Guan C, Tsay YF, Moran N, Oh CJ, An CS, Demchenko KN, Pawlowski K, Lee Y (2004) A nodule-specific dicarboxylate transporter from alder is a member of the peptide transporter family. Plant Physiol 134: 969-798.
27. Kannenberg EL, Brewin NJ (1989) Expression of a cell-surface antigen from Rhizobium leguminosarum 3841 is regulated by oxygen and pH. J Bacteriol 171: 4543-4548.
28. Keller F, Pharr DM (1996) Metabolism of carbohydrates in sinks and sources: galactosyl-sucrose oligosaccharides. In: Zamski E, Schaffer AA (eds) Photoassimilate distribution in plants and crops. Marcel Dekker, New York, pp 115-184.
29. 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.
30. Kim J-Y, Mahé A, Brangeon J, Prioul J-L (2000) A maize vacuolar invertase, IVR2, is induced by water stress, organ/tissue specificity and diurnal modulation of expression. Plant Physiol 124: 71-84.
31. Knop C, Voitsekhovskaja O, Lohaus G (2001) Sucrose transporters in two members of the Scrophulariaceae with different types of transport sugar. Planta 213: 80-91.
32. Krausgrill S, Sander A, Greiner S, Weil M, Rausch T (1996) Regulation of cell wall invertase by a proteinaceous inhibitor. J Exp Bot 47: 1193-1198.
33. Liu QQ, Berry AM (1991) Localization and characterization of pectic polysaccharides in roots and root-nodules of Ceanothus spp. during intercellular infection by Frankia. Protoplasma 163: 93-101.
34. Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66-69.
35. Ma F, Peterson CA (2001) Frequencies of plasmodesmata in Allium cepa L. roots: implications for solute transport pathways. J Exp Bot 52: 1051-1061.
36. Malek W (1988) Microscopic structure of ineffective alfalfa nodules formed by auxotrophic mutants of Rhizobium meliloti. J Basic Microbiol 28: 651-658.
37. Mellor RB (1989) Bacteroides in the rhizobium-legume symbiosis inhabit a plant internal lytic compartment-implications for other microbial endosymbioses. J Exp Bot 40: 831-839.
38. Newcomb W, Pankhurst CE (1982) Fine structure of actinorhizal nodules of Coriaria arborea (Coriariaceae). New Zeal J Bot 20: 93-103.
39. Normand P, Gouy M, Cournoyer B, Simonet R (1992) Nucleotide sequence of nifD from Frankia alni strain ARI3-phylogenetic inferences. Mol Biol Evol 9: 495-506.
40. Patrick JW (1997) Phloem unloading-sieve element unloading and post-sieve element transport. Annu Rev Plant Physiol Plant Mol Biol 48: 191-222.
41. Pawlowski K, Bisseling T (1996) Rhizobial and actinorhizal symbioses: what are the shared features? Plant Cell 8: 1899-1913.
42. Pawlowski K, Swensen S, Guan C, Hadri A-E, Berry AM, Bisseling T (2003) Distinct patterns of symbiosis-related gene expression in actinorhizal nodules from different plant families. Mol Plant Microbe Interact 16: 796-807.
43. Pawlowski K, Jacobsen KR, Alloisio N, Denison RF, Klein M, Winzer T, Sirrenberg A, Guan C, Berry AM (2007) Truncated hemoglobins in actinorhizal nodules of Datisca glomerata. Plant Biol 9: 776-785.
44. Reiter WD, Chapple C, Somerville CR (1997) Mutants of Arabidopsis thaliana with altered cell wall polysaccharide composition. Plant J 12: 335-345.
45. Ribeiro A, Akkermans ADL, van Kammen A, Bisseling T, Pawlowski K (1995) A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development. Plant Cell 7: 785-794.
46. Roitsch T, Bittner M, Godt DE (1995) Induction of apoplastic invertase of Chenopodium rubrum by d-glucose and a glucose analog and tissue-specific expression suggest a role in sink-source regulation. Plant Physiol 108: 285-294.
47. Rolletschek H, Borisjuk L, Koschorreck M, Wobus U, Weber H (2002) Legume embryos develop in a hypoxic environment. J Exp Bot 53: 1099-1107.
48. Ross HA, Davies HV (1992) Purification and characterization of sucrose synthase from the cotyledons of Vicia faba L. Plant Physiol 100: 1008-1013.
49. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Plainview.
50. +/monosaccharide cotransporter from Nicotianatabacum-cloning and heterologous expression in bakers-yeast. Plant J 4: 601-610.
51. Sauer N, Stolz J (1994) SUC1 and SUC2-2 sucrose transporters from Arabidopsis thaliana-expression and characterization in bakers yeast and identification of the histidine-tagged protein. Plant J 6: 67-77.
52. Schneidereit A, Scholz-Starke J, Büttner M (2003) Functional characterization and expression analyses of the glucose-specific AtSTP9 monosaccharide transporter in pollen of Arabidopsis. Plant Physiol 133: 182-190.
53. Schubert M, Melnikova AN, Mesecke N, Zubkova EK, Fortte R, Batashev DR, Barth I, Sauer N, Gamalei YuV, Mamushina NS, Tietze L, Voitsekhovskaja OV, Pawlowski K (2010) Two novel disaccharides, rutinose and methylrutinose, are involved in carbon metabolism in Datisca glomerata. Planta 231: 507-521.
54. Selker JML (1988) Three-dimensional organization of uninfected tissue in soybean root nodules and its reaction to cell specialization in the central region. Protoplasma 147: 178-190.
55. 2+-ATPases. Nature 319: 689-693.
56. Sherson SM, Alford HL, Forbes SM, Wallace G, Smith SM (2003) Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis. J Exp Bot 54: 525-531.
57. Stadler R, Brandner J, Schulz A, Gahrtz M, Sauer N (1995) Phloem loading by the PmSUC2 sucrose carrier from Plantago major occurs into companion cells. Plant Cell 7: 1545-1554.
58. Stadler R, Büttner M, Ache P, Hedrich R, Ivashikina N, Melzer M, Shearson SM, Smith SM, Sauer N (2003) Diurnal and light-regulated expression of AtSTP1 in guard cells of Arabidopsis. Plant Physiol 133: 528-537.
59. + symporter in lipid vesicles and purification of the histidine tagged protein from transgenic Saccharomyces cerevisiae. Plant J 6: 225-233.
60. Streeter JG (1995) Recent developments in carbon transport and metabolism in symbiotic systems. Symbiosis 19: 175-196.
61. Sturm A, Tang G-Q (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4: 401-407.
62. Sung S-J, Xu D-P, Black CC (1989) Identification of actively filling sucrose sinks. Plant Physiol 89: 1117-1121.
63. Viola R, Roberts AG, Haupt S, Gazzani S, Hancock RD, Marmiroli N, Machray GC, Oparka KJ (2001) Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. Plant Cell 13: 385-398.
64. Weber H, Borisjuk L, Heim U, Sauer N, Wobus U (1997a) A role for sugar transporters during seed development: molecular characterization of a monosaccharide and a sucrose carrier in fava bean seeds. Plant Cell 9: 895-908.
65. Weber H, Borisjuk L, Wobus U (1997b) Sugar import and metabolism during seed development. Trends Plant Sci 2: 169-174.
66. Weig A, Franz J, Sauer N, Komor E (1994) Isolation of a family of cDNA clones from Ricinus communis L. with close homology to the monosaccharide carriers. J Plant Physiol 143: 178-183.
67. Wieczorke R, Krampe S, Weierstall T, Freidel K, Hollenberg CP, Boles E (1999) Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae. FEBS Lett 31: 123-128.
68. Winter H, Huber JL, Huber SC (1998) Identification of sucrose synthase as an actin-binding protein. FEBS Lett 430: 205-208.
69. Zeng Y, Wu Y, Avigne WT, Koch KE (1999) Rapid repression of maize invertase by low oxygen. Invertase/sucrose synthase balance, sugar signaling potential, and seedling survival. Plant Physiol 121: 599-608.
70. Zimmermann MH, Ziegler H (1975) Transport in plants. I. Phloem transport. In: Zimmermann MH, Milburn JA (eds) Encyclopedia of plant physiology, New Series, vol 1. Springer, Berlin, pp 480-503.