The potato-specific apyrase is apoplastically localized and has influence on gene expression, growth, and development

Plant Physiology

Volumn 147, Issue 3, 2008, Pages 1092-1109

  Riewe, David ^a   Grosman, Lukasz ^a   Fernie, Alisdair R ^a   Wucke, Cornelia ^a   Geigenberger, Peter ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA; PROKARYOTA; SOLANUM TUBEROSUM; TUBER (TRUFFLE);

APYRASE; GREEN FLUORESCENT PROTEIN; MESSENGER RNA;

ARTICLE; CONSENSUS SEQUENCE; ENZYMOLOGY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR CLONING; PLANT EPIDERMIS; PLANT LEAF; PLANT TUBER; POTATO; PROMOTER REGION; TRANSGENIC PLANT;

APYRASE; CLONING, MOLECULAR; CONSENSUS SEQUENCE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GREEN FLUORESCENT PROTEINS; PLANT EPIDERMIS; PLANT LEAVES; PLANT TUBERS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS (GENETICS); RNA, MESSENGER; SOLANUM TUBEROSUM;

EID: 51549099085     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.117564     Document Type: Article

References (75)

1. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402
2. Baumberger N, Ringli C, Keller B (2001) The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Genes Dev 15: 1128-1139
3. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol 57: 289-300
4. Boudart G, Jamet E, Rossignol M, Lafitte C, Borderies G, Jauneau A, Esquerre-Tugaye MT, Pont-Lezica R (2005) Cell wall proteins in apoplastic fluids of Arabidopsis thaliana rosettes: identification by mass spectrometry and bioinformatics. Proteomics 5: 212-221
5. Che M, Nishida T, Gatmaitan Z, Arias IM (1992) A nucleoside transporter is functionally linked to ectonucleotidases in rat liver canalicular membrane. J Biol Chem 267: 9684-9688
6. Chivasa S, Ndimba BK, Simon WJ, Lindsey K, Slabas AR (2005) Extracellular ATP functions as an endogenous external metabolite regulating plant cell viability. Plant Cell 17: 3019-3034
7. Cohn JR, Uhm T, Ramu S, Nam YW, Kim DJ, Penmetsa RV, Wood TC, Denny RL, Young ND, Cook DR, et al (2001) Differential regulation of a family of apyrase genes from Medicago truncatula. Plant Physiol 125: 2104-2119
8. Day RB, McAlvin CB, Loh JT, Denny RL, Wood TC, Young ND, Stacey G (2000) Differential expression of two soybean apyrases, one of which is an early nodulin. Mol Plant Microbe Interact 13: 1053-1070
9. Degenkolbe T, Hannah MA, Freund S, Hincha DK, Heyer AG, Kohl KI (2005) A quality-controlled microarray method for gene expression profiling. Anal Biochem 346: 217-224
10. Dische Z (1962) General color reactions. Methods Carbohydr Chem 1: 478-492
11. Dunkley TP, Watson R, Griffin JL, Dupree P, Lilley KS (2004) Localization of organelle proteins by isotope tagging (LOPIT). Mol Cell Proteomics 3: 1128-1134
12. Englyst HN, Cummings JH (1984) Simplified method for the measurement of total non-starch polysaccharides by gas-liquid chromatography of constituent sugars as alditol acetates. Analyst 109: 937-942
13. Etzler ME, Kalsi G, Ewing NN, Roberts NJ, Day RB, Murphy JB (1999) A nod factor binding lectin with apyrase activity from legume roots. Proc Natl Acad Sci USA 96: 5856-5861
14. Fanta N, Anich M, Mancilla M, Kettlum AM, Valenzuela MA, Traverso-Cori A (1988) Starch, adenine nucleotides and apyrase changes during potato tuber development. Arch Biol Med Exp (Santiago) 21: 129-133
15. Farran I, Sanchez-Serrano JJ, Medina JF, Prieto J, Mingo-Castel AM (2002) Targeted expression of human serum albumin to potato tubers. Transgenic Res 11: 337-346
16. Farre EM, Tiessen A, Roessner U, Geigenberger P, Trethewey RN, Willmitzer L (2001) Analysis of the compartmentation of glycolytic intermediates, nucleotides, sugars, organic acids, amino acids, and sugar alcohols in potato tubers using a nonaqueous fractionation method. Plant Physiol 127: 685-700
17. Fecht-Christoffers MM, Fuhrs H, Braun HP, Horst WJ (2006) The role of hydrogen peroxide-producing and hydrogen peroxide-consuming peroxidases in the leaf apoplast of cowpea in manganese tolerance. Plant Physiol 140: 1451-1463
18. Fettke J, Poeste S, Eckermann N, Tiessen A, Pauly M, Geigenberger P, Steup M (2005) Analysis of cytosolic heteroglycans from leaves of transgenic potato (Solanum tuberosum L.) plants that under- or overexpress the Pho 2 phosphorylase isozyme. Plant Cell Physiol 46: 1987-2004
19. Filisetti-Cozzi TM, Carpita NC (1991) Measurement of uronic acids without interference from neutral sugars. Anal Biochem 197: 157-162
20. Geigenberger P (2003) Regulation of sucrose to starch conversion in growing potato tubers. J Exp Bot 54: 457-465
21. Geigenberger P, Fernie AR (2006) Starch biosynthesis in the potato tuber. In Food Biochemistry and Food Processing. Blackwell Publishing, Oxford, pp 253-270
22. Geigenberger P, Hajirezaei M, Geiger M, Deiting U, Sonnewald U, Stitt M (1998) Overexpression of pyrophosphatase leads to increased sucrose degradation and starch synthesis, increased activities of enzymes for sucrose-starch interconversions, and increased levels of nucleotides in growing potato tubers. Planta 205: 428-437
23. Geigenberger P, Stitt M (1993) Sucrose synthase catalyzes a readily reversible reaction in vivo in developing potato tubers and other plant tissues. Planta 189: 329-339
24. Geigenberger P, Stitt M, Fernie AR (2004) Metabolic control analysis and regulation of the conversion of sucrose to starch in growing potato tubers. Plant Cell Environ 27: 655-673
25. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80
26. Gleave AP (1992) A versatile binary vector system with a T-DNA organizational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol Biol 20: 1203-1207
27. Hall Q, Cannon MC (2002) The cell wall hydroxyproline-rich glycoprotein RSH is essential for normal embryo development in Arabidopsis. Plant Cell 14: 1161-1172
28. Handa M, Guidotti G (1996) Purification and cloning of a soluble ATP-diphosphohydrolase (apyrase) from potato tubers (Solanum tuberosum). Biochem Biophys Res Commun 218: 916-923
29. Hsieh HL, Song CJ, Roux SJ (2000) Regulation of a recombinant pea nuclear apyrase by calmodulin and casein kinase II. Biochim Biophys Acta 1494: 248-255
30. Jelitto T, Sonnewald U, Willmitzer L, Hajirezeai M, Stitt M (1992) Inorganic pyrophosphate content and metabolites in potato and tobacco plants expressing Escherichia coli pyrophosphatase in their cytosol. Planta 188: 238-244
31. Kalckar HM (1944) Adenylpyrophosphatase and myokinase. J Biol Chem 153: 355-367
32. Kalsi G, Etzler ME (2000) Localization of a Nod factor-binding protein in legume roots and factors influencing its distribution and expression. Plant Physiol 124: 1039-1048
33. Kettlun AM, Uribe L, Calvo V, Silva S, Rivera J, Mancilla M, Valenzuela MA, Traversocori A (1982) Properties of 2 apyrases from Solanum tuberosum. Phytochemistry 21: 551-558
34. Kim SY, Sivaguru M, Stacey G (2006) Extracellular ATP in plants: visualization, localization, and analysis of physiological significance in growth and signaling. Plant Physiol 142: 984-992
35. Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 102: 11118-11123
36. Liu XJ, Prat S, Willmitzer L, Frommer WB (1990) Cis regulatory elements directing tuber-specific and sucrose-inducible expression of a chimeric class-I patatin promoter GUS-gene fusion. Mol Gen Genet 223: 401-406
37. Loef I, Stitt M, Geigenberger P (1999) Orotate leads to a specific increase in uridine nucleotide levels and a stimulation of sucrose degradation and starch synthesis in discs from growing potato tubers. Planta 209: 314-323
38. Marcus AJ, Broekman MJ, Drosopoulos JH, Islam N, Alyonycheva TN, Safier LB, Hajjar KA, Posnett DN, Schoenborn MA, Schooley KA, et al (1997) The endothelial cell ecto-ADPase responsible for inhibition of platelet function is CD39. J Clin Invest 99: 1351-1360
39. Mattanovich D, Ruker F, Machado AD, Laimer M, Regner F, Steinkellner H, Himmler G, Katinger H (1989) Efficient transformation of Agrobacterium spp by electroporation. Nucleic Acids Res 17: 6747
40. McAlvin CB, Stacey G (2005) Transgenic expression of the soybean apyrase in Lotus japonicus enhances nodulation. Plant Physiol 137: 1456-1462
41. Merkouropoulos G, Shirsat AH (2003) The unusual Arabidopsis extensin gene atExt1 is expressed throughout plant development and is induced by a variety of biotic and abiotic stresses. Planta 217: 356-366
42. Molnar J, Lorand L (1961) Studies on apyrases. Arch Biochem Biophys 93: 353-363
43. Neckelmann G, Orellana A (1998) Metabolism of uridine 5′-diphosphate-glucose in Golgi vesicles from pea stems. Plant Physiol 117: 1007-1014
44. Oliver SN, Tiessen A, Fernie AR, Geigenberger P (2008) Decreased expression of plastidial adenylate kinase in potato tubers results in an enhanced rate of respiration and a stimulation of starch synthesis that is attributable to post-translational redox-activation of ADP-glucose pyrophosphorylase. J Exp Bot 59: 315-325
45. Orellana A, Neckelmann G, Norambuena L (1997) Topography and function of Golgi uridine-5′-diphosphatase from pea stems. Plant Physiol 114: 99-107
46. Plesner L (1995) Ecto-ATPases: identities and functions. Int Rev Cytol 158: 141-214
47. Riewe D, Grosman L, Zauber H, Wucke C, Fernie AR, Geigenberger P (2008) Metabolic and developmental adaptations of growing potato tubers in response to specific manipulations of the adenylate energy status. Plant Physiol 146: 1579-1598
48. Roberts K, Shirsat AH (2006) Increased extensin levels in Arabidopsis affect inflorescence stem thickening and height. J Exp Bot 57: 537-545
49. Roberts NJ, Brigham J, Wu B, Murphy JB, Volpin H, Phillips DA, Etzler ME (1999) A Nod factor-binding lectin is a member of a distinct class of apyrases that may be unique to the legumes. Mol Gen Genet 262: 261-267
50. Rocha-Sosa M, Sonnewald U, Frommer W, Stratmann M, Schell J, Willmitzer L (1989) Both developmental and metabolic signals activate the promoter of a class I patatin gene. EMBO J 8: 23-29
51. Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie A (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13: 11-29
52. Rotter A, Usadel B, Baebler S, Stitt M, Gruden K (2007) Adaptation of the MapMan ontology to biotic stress responses: application in solanaceous species. Plant Methods 3: 10
53. Rumeau D, Maher EA, Kelman A, Showalter AM (1990) Extensin and phenylalanine ammonia-lyase gene expression altered in potato tubers in response to wounding, hypoxia, and Erwinia carotovora infection. Plant Physiol 93: 1134-1139
54. Serrato AJ, Perez-Ruiz JM, Spinola MC, Cejudo FJ (2004) A novel NADPH thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana. J Biol Chem 279: 43821-43827
55. Smyth GK, Michaud J, Scott HS (2005) Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21: 2067-2075
56. Sohlenkamp C, Wood CC, Roeb GW, Udvardi MK (2002) Characterization of Arabidopsis AtAMT2, a high-affinity ammonium transporter of the plasma membrane. Plant Physiol 130: 1788-1796
57. Song CJ, Steinebrunner I, Wang X, Stout SC, Roux SJ (2006) Extracellular ATP induces the accumulation of superoxide via NADPH oxidases in Arabidopsis. Plant Physiol 140: 1222-1232
58. Steinebrunner I, Jeter C, Song C, Roux SJ (2000) Molecular and biochemical comparison of two different apyrases from Arabidopsis thaliana. Plant Physiol Biochem 38: 913-922
59. Steinebrunner I, Wu J, Sun Y, Corbett A, Roux SJ (2003) Disruption of apyrases inhibits pollen germination in Arabidopsis. Plant Physiol 131: 1638-1647
60. Sweetlove LJ, Muller-Rober B, Willmitzer L, Hill SA (1999) The contribution of adenosine 5′-diphosphoglucose pyrophosphorylase to the control of starch synthesis in potato tubers. Planta 209: 330-337
61. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914-939
62. Thomas C, Rajagopal A, Windsor B, Dudler R, Lloyd A, Roux SJ (2000) A role for ectophosphatase in xenobiotic resistance. Plant Cell 12: 519-533
63. Thomas C, Sun Y, Naus K, Lloyd A, Roux S (1999) Apyrase functions in plant phosphate nutrition and mobilizes phosphate from extracellular ATP. Plant Physiol 119: 543-551
64. Tiessen A, Hendriks JHM, Stitt M, Branscheid A, Gibon Y, Farre EM, Geigenberger P (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14: 2191-2213
65. Tjaden J, Mohlmann T, Kampfenkel K, Henrichs G, Neuhaus HE (1998) Altered plastidic ATP/ADP-transporter activity influences potato (Solanum tuberosum L.) tuber morphology, yield and composition of tuber starch. Plant J 16: 531-540
66. Todorov LD, Mihaylova-Todorova S, Westfall TD, Sneddon P, Kennedy C, Bjur RA, Westfall DP (1997) Neuronal release of soluble nucleotidases and their role in neurotransmitter inactivation. Nature 387: 76-79
67. Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32: 420-424
68. Voelker C, Schmidt D, Mueller-Roeber B, Czempinski K (2006) Members of the Arabidopsis AtTPK/KCO family form homomeric vacuolar channels in planta. Plant J 48: 296-306
69. Wesley SV, Helliwell CA, Smith NA, Wang MB, Rouse DT, Liu Q, Gooding PS, Singh SP, Abbott D, Stoutjesdijk PA, et al (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 27: 581-590
70. Windsor B, Roux SJ, Lloyd A (2003) Multiherbicide tolerance conferred by AtPgp1 and apyrase overexpression in Arabidopsis thaliana. Nat Biotechnol 21: 428-433
71. Wolf C, Hennig M, Romanovicz D, Steinebrunner I (2007) Developmental defects and seedling lethality in apyrase AtAPY1 and AtAPY2 double knockout mutants. Plant Mol Biol 64: 657-672
72. Wu H, de Graaf B, Mariani C, Cheung AY (2001) Hydroxyproline-rich glycoproteins in plant reproductive tissues: structure, functions and regulation. Cell Mol Life Sci 58: 1418-1429
73. Wu J, Steinebrunner I, Sun Y, Butterfield T, Torres J, Arnold D, Gonzalez A, Jacob F, Reichler S, Roux SJ (2007) Apyrases (nucleoside triphosphate-diphosphohydrolases) play a key role in growth control in Arabidopsis. Plant Physiol 144: 961-975
74. Zhang L, Greiten C, Schmitz I, Haferkamp I, Neuhaus HE, Hausler RE, Flugge UI, Ludewig F (2006) Impact of glucose 6-phosphate import into amyloplasts on potato tuber starch content. In DP Bourque, ed, 8th International Congress of Plant Molecular Biology, Adelaide, Australia. International Society for Plant Molecular Biology, Athens, GA, p 93
75. Zrenner R, Willmitzer L, Sonnewald U (1993) Analysis of the expression of potato uridinediphosphate-glucose pyrophosphorylase and its inhibition by antisense RNA. Planta 190: 247-252