RNA interference-mediated repression of cell wall invertase impairs defense in source leaves of tobacco

Plant Physiology

Volumn 147, Issue 3, 2008, Pages 1288-1299

  Essmann, Jutta ^a   Schmitz Thom, Ina ^a   Schön, Hardy ^a   Sonnewald, Sophia ^b   Weis, Engelbert ^a   Scharte, Judith ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b Institute for Biology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTIANA TABACUM; PHYTOPHTHORA; PHYTOPHTHORA NICOTIANAE;

BETA FRUCTOFURANOSIDASE; CALLOSE; GLUCAN; HEXOSE; SUCROSE;

ARTICLE; CARBOHYDRATE METABOLISM; CELL DEATH; CELL WALL; ENZYMOLOGY; HOST PARASITE INTERACTION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; PHYTOPHTHORA; PLANT DISEASE; PLANT LEAF; RNA INTERFERENCE; TOBACCO; TRANSGENIC PLANT;

BETA-FRUCTOFURANOSIDASE; CARBOHYDRATE METABOLISM; CELL DEATH; CELL WALL; GLUCANS; HEXOSES; HOST-PARASITE INTERACTIONS; MOLECULAR SEQUENCE DATA; PHYTOPHTHORA; PLANT DISEASES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; RNA INTERFERENCE; SUCROSE; TOBACCO;

EID: 51549114743     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.121418     Document Type: Article

References (63)

1. Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant pathogen interactions. J Exp Bot 58: 4019-4026
2. Biemelt S, Sonnewald U (2006) Plant-microbe interactions to probe regulation of plant carbon metabolism. J Plant Physiol 163: 307-318
3. Chen S, Hajirezaei MR, Zanor MI, Hornyik C, Debast S, Lacomme C, Fernie AR, Sonnewald U, Börnke F (2008) RNA interference-mediated repression of Suc-phosphatase in transgenic potato tubers (Solanum tuberosum) strongly affects the hexose-to-Suc ratio upon cold storage with only minor effects on total soluble carbohydrate accumulation. Plant Cell Environ 31: 165-176
4. Colas V, Conrod S, Venard P, Keller H, Ricci P, Panabieres F (2001) Elicitin genes expressed in vitro by certain tobacco isolates of Phytophthora parasitica are down regulated during compatible interactions. Mol Plant Microbe Interact 14: 326-335
5. Conrath U, Linke C, Jeblick W, Geigenberger P, Quick WP, Neuhaus HE (2003) Enhanced resistance to Phytophthora infestans and Alternaria solani in leaves and tubers, respectively, of potato plants with decreased activity of the plastidic ATP/ADP transporter. Planta 217: 75-83
6. Deblaere R, Bytebier B, DeGreve H, Beboeck F, Schell J, Van Montagu M, Leemanns J (1985) Efficient octopine Ti plasmid-derived vectors for Agrobacterium mediated gene transfer to plants. Nucleic Acids Res 13: 4777-4788
7. De Coninck B, Le Roy K, Francis I, Clerens S, Vergauwen R, Halliday AM, Smith SM, Van Laere A, Van den Ende W (2005) Arabidopsis AtcwINV3 and 6 are not invertases but are fructan exohydrolases (FEHs) with different substrate specificities. Plant Cell Environ 28: 432-443
8. Ehness R, Ecker M, Godt D, Roitsch T (1997) Glucose and stress independently regulate source/sink relations and defence mechanisms via signal transduction pathways involving protein phosphorylation. Plant Cell 9: 1825-1841
9. Erwin DC, Ribeiro OK (1996) Phytophthora Diseases Worldwide. APS Press, St. Paul
10. Fridman D, Zamir D (2003) Functional divergence of a syntenic invertase gene family in tomato, potato, and Arabidopsis. Plant Physiol 131: 603-609
11. Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, Poinssot B, Wendehenne D, Pugin A (2006) Early signaling events induced by elicitors of plant defenses. Mol Plant Microbe Interact 19: 711-724
12. Geigenberger P, Kolbe A, Tiessen A (2005) Redox regulation of carbon storage and partitioning in response to light and sugars. J Exp Bot 56: 1469-1479
13. Geigenberger P, Müller-Röber B, Stitt M (1999) Contribution of adenosine 5′-diphosphoglucose pyrophosphorylase to the control of starch synthesis is decreased by water stress in growing potato tubers. Planta 209: 338-345
14. Gibon Y, Bläsing OE, Palacios-Rojas N, Pankovic D, Hendriks JHM, Fisahn J, Höhne M, Günther M, Stitt M (2004) Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant J 39: 847-862
15. Godt DE, Roitsch T (1997) Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism. Plant Physiol 115: 273-282
16. Goetz M, Roitsch T (1999) The different pH-optima and substrate specificities of extracellular and vacuolar invertases are determined by a single amino acid substitution. Plant J 20: 707-711
17. Gómez-Gómez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18: 277-284
18. Greiner S, Weil M, Krausgrill S, Rausch T (1995) A tobacco cDNA coding for cell-wall invertase. Plant Physiol 108: 825-826
19. Hardham AR (2007) Cell biology of plant-oomycete interactions. Cell Microbiol 9: 1-39
20. Herbers K, Meuwly P, Frommer W, Metraux J, Sonnewald U (1996) Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell 8: 793-803
21. Herbers K, Takahata Y, Melzer M, Mock HP, Hajirezaei M, Sonnewald U (2000) Regulation of carbohydrate partitioning during the interaction of potato virus Y with tobacco. Mol Plant Pathol 1: 51-59
22. Horsfall J (1975) The story of a nonconformist. Annu Rev Phytopathol 13: 1-13
23. Horsfall J, Dimond A (1957) Interactions of tissue sugar, growth substances and disease susceptibility. Z Pflanzenkr Pflanzenschutz 64: 415-421
24. Huang LF, Bocock PN, Davis JM, Koch KE (2007) Regulation of invertase: a 'suite' of transcriptional and post-transcriptional mechanisms. Funct Plant Biol 34: 499-507
25. Ji X, Van den Ende W, Van Laere A, Cheng S, Benett J (2005) Structure, evolution, and expression of the two invertase gene families of rice. J Mol Evol 60: 615-634
26. Judelson HS, Blanco FA (2005) The spores of Phytophthora: weapons of the plant destroyer. Nat Rev Microbiol 3: 47-58
27. Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193-195
28. Kim M, Lim JH, Ahn CS, Park K, Kim GT, Kim WT, Pai HS (2006) Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana. Plant Cell 18: 2341-2355
29. Kingston-Smith AH, Galtier N, Pollock CJ, Foyer CH (1998) Soluble acid invertase activity in leaves is independent of species differences in leaf carbohydrates, diurnal sugar profiles and paths of phloem loading. New Phytol 139: 283-292
30. Koch K (2004) Suc metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7: 235-246
31. Kunst A, Draeger B, Ziegenhorn J (1984) D-Glc. In HU Bergmeyer, J Bergmeyer, M Graßl, eds, Methods of Enzymatic Analysis, Ed 3, Vol 4. Verlag Chemie, Weinheim, Germany, pp 1469-1473
32. Le QL, Lorenz Y, Scheurer S, Fötisch K, Enrique E, Bartra J, Biemelt S, Vieths S, Sonnewald U (2006) Design of tomato fruits with reduced allergenicity by dsRNAi-mediated inhibition of ns-LTP (Lyc e 3) expression. Plant Biotechnol J 4: 231-242
33. Leidreiter K, Heineke D, Heldt HW, Müller-Röber B, Sonnewald U, Willmitzer L (1995) Leaf-specific antisense inhibition of starch biosynthesis in transgenic potato plants leads to an increase in photoassimilate export from source leaves during the light period. Plant Cell Physiol 36: 615-624
34. Logemann J, Schell J, Willmitzer L (1987) Improved method for the isolation of RNA from plant tissues. Anal Biochem 163: 16-20
35. Lohaus G, Pennewiss K, Sattelmacher B, Hussmann M, Muehling K (2001) Is the infiltration-centrifugation technique appropriate for the isolation of apoplastic fluid? A critical evaluation with different plant species. Physiol Plant 111: 457-465
36. Löw R, Rausch T (1996) Detection of nucleic acids with biotinylated PCR-amplified probes. In T Meier, F Fahrenholz, eds, A Laboratory Guide to Biotinin-Labelling in Biomolecule Analysis. Birkhäuser Verlag, Basel, pp 201-213
37. Maor R, Shirasu K (2005) The arms race continues: battle strategies between plants and fungal pathogens. Curr Opin Microbiol 8: 399-404
38. Müller-Röber BT, Sonnewald U, Willmitzer L (1992) Inhibition of ADP-Glc pyrophosphorylase leads to sugar storing tubers and influences tuber formation and expression of tuber storage protein genes. EMBO J 11: 1229-1238
39. Murillo I, Roca R, Bortolotti C, Segundo BS (2003) Engineering photoassimilate partitioning in tobacco plants improves growth and productivity and provides pathogen resistance. Plant J 36: 330-341
40. Nguyen-Quoc B, Foyer CH (2001) A role for 'futile cycles' involving invertase and Suc synthase in Suc metabolism of tomato fruit. J Exp Bot 52: 881-889
41. Pugin A, Frachisse JM, Tavernier E, Bligny R, Gout E, Douce R, Guern J (1997) Early events induced by the elicitor cryptogein in tobacco cells: involvement of a plasma membrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway. Plant Cell 9: 2077-2091
42. Rat P, Osseni R, Christen MO, Thevenin M, Warnet J-M, Adolphe M (1997) Microtitration fluorimetric assays on living cells (MiFALC tests): new tools for screening in cell pharmacotoxicology. In LFM Van Zutphen, M Balls, eds, Animal Alternatives, Welfare and Ethics. Elsevier, Paris, pp 813-825
43. Roitsch T (1999) Source-sink regulation by sugar and stress. Curr Opin Plant Biol 2: 198-206
44. Roitsch T, Balibrea ME, Hofmann M, Proels R, Sinha AK (2003) Extracellular invertase: key metabolic enzyme and PR protein. J Exp Bot 54: 513-524
45. Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9: 606-613
46. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57: 675-709
47. Rongrong L, Shaohua X, Jialin L, Yuanlei H, Zhongping L (2006) Expression profile of a PAL gene from Astragalus membranaceus var. Mongholicus and its crucial role in flux into flavonoid biosynthesis. Plant Cell Rep 25: 705-710
48. Rosahl S, Schmidt R, Schell J, Willmitzer L (1987) Expression of a tuber specific storage protein in transgenic tobacco plants: demonstration of an esterase activity. EMBO J 6: 1155-1159
49. Scharte J, Schön H, Weis E (2005) Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae. Plant Cell Environ 28: 1421-1435
50. Schweizer P, Pokorny J, Schulze-Lefert P, Dudler R (2000) Technical advance. Double-stranded RNA interferes with gene function at the single-cell level in cereals. Plant J 24: 895-903
51. Seo YS, Cho JI, Lee SK, Ryu HS, Han M, Hahn TR, Sonnewald U, Jeon JS (2007) Current insights into the primary carbon metabolic flux that occurs in plants undergoing a defense response. Plant Stress 1: 42-49
52. 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
53. Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and Suc partitioning. Plant Physiol 121: 1-8
54. Swarbrick PJ, Schulze-Lefert P, Scholes JD (2006) Metabolic consequences of susceptibility and resistance (race specific and broad-spectrum) in barley leaves challenged with powdery mildew. Plant Cell Environ 29: 1061-1076
55. Takemoto D, Hardham AR (2004) The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol 136: 3864-3876
56. Takemoto D, Jones DA, Hardham AR (2003) GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J 33: 775-792
57. Taler D, Galperin M, Benjamin I, Cohen Y, Kenigsbuch D (2004) Plant eR genes encoding for photorespiratory enzymes confer resistance against disease. Plant Cell 16: 172-184
58. Tomos AD, Sharrock RA (2001) Cell sampling and analysis (SiCSA): metabolites measured at single cell resolution. J Exp Bot 52: 623-630
59. Voegele RT, Wirsel SGR, Möll U, Lechner M, Mendgen K (2006) Cloning and characterization of a novel invertase from the obligate biotroph "Uromyces fabae" and analysis of expression patterns of host and pathogen invertases in the course of infection. Mol Plant Microbe Interact 19: 625-634
60. von Broembsen SL, Deacon JW (1996) Germination and further zoospore release from zoospore cysts of Phytophthora parasitica. Mycol Res 100: 1498-1504
61. von Schaewen A, Stitt M, Schmidt R, Willmitzer L (1990) Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate, inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. EMBO J 9: 3033-3044
62. Weil M, Krausgrill S, Schuster A, Rausch T (1994) A 17-kDa Nicotiana tabacum cell-wall peptide acts as an in vitro inhibitor of the cell-wall isoform of acid invertase. Planta 193: 438-445
63. Zeeman SC, Smith SM, Smith AM (2007) The diurnal metabolism of leaf starch. Biochem J 401: 13-28