Infection of Arabidopsis thaliana leaves with Albugo Candida (white blister rust) causes a reprogramming of host metabolism

Molecular Plant Pathology

Volumn 1, Issue 2, 2000, Pages 99-113

  Chou, Hsueh Mei ^a   Bundock, Nicholas ^a   Rolfe, Stephen A ^a   Scholes, Julie D ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0002241571     PISSN: 14646722     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1364-3703.2000.00013.x     Document Type: Article

References (57)

1. Altschul, S.F., Madden, T.L., Schäffen, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25, 3389-3402.
2. Balachandran, S., Osmond, C.B. and Daley, P.P. (1994) Diagnosis of the earliest strain-specific interactions between tobacco mosaic virus and chloroplasts of tobacco leaves in vivo by means of chlorophyll fluorescence imaging. Plant Physiol. 104, 1059-1065.
3. Basse, C.W., Bock, K. and Boiler, T. (1992) Elicitors and suppressors of the defense response in tomato cells. J. Biol. Chem. 267, 10258-10265.
4. Benhamou, N., Grenier, J. and Chrispeels, M.J. (1991) Accumulation of β-fructosidase in the cell walls of tomato roots following infection by a fungal wilt pathogen. Plant Physiol. 97, 739-750.
5. Brem, S., Rast, D.M. and Ruffner, H.P. (1986) Partitioning of photosynthate in leaves of Vitis vinifera infected with Uncinula necator or Plasmopara viticola. Physiol. Mol. Plant Pathol 29, 285-291.
6. Dong, X., Mindrinos, M., Davis, K.R. and Ausubel, F.M. (1991) Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell, 3, 61-72.
7. Ehness, R. and Roitsch, T. (1997) Co-ordinated induction of mRNAs for extracellular invertase and a glucose transporter in Chenopodium rubrum by cytokinins. Plant J. 11, 539-548.
8. Eschrich, W. (1980) Free space invertase, its possible role in phloem unloading. Ber. Dtsch. Bot. Ges, 93, 363-378.
9. Farrar, J.F. and Lewis, D.H. (1987) Nutrient relations in biotrophic infections. In: Fungal Infection of Plants (Pegg, G. and Ayres, P., eds). Cambridge, UK: Cambridge University Press, pp. 92-132.
10. Faye, L. (1981) A new enzymatic staining method for the detection of radish beta-fructosidase in gel electrophoresis. Anal. Biochem. 112, 90-95.
11. Genty, B., Briantais, J. and Baker, N.R. (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica Biophysica Acta, 990, 87-92.
12. Godt, D.E. and 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.
13. Heisterüber, D., Schulte, P. and Moerschbacher, B.M. (1994) Soluble carbohydrates and invertase activity in stem rust-infected, resistant and susceptible near-isogenic wheat leaves. Physiol. Mol. Plant Pathol. 44, 111-123.
14. Herbers, K., Meuwly, P., Frommer, W.B., Métraux, J. and 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.
15. Herbers, K. and Sonnewald, U. (1998) Altered gene expression brought about by inter-and intracellularly formed hexoses and its possible implications for plant-pathogen interactions. J. Plant Res. 111, 323-328.
16. Jang, J., León, P., Zhou, L. and Sheen, J. (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9, 5-19.
17. Johnson, R. and Ryan, C.A. (1990) Wound-inducible potato inhibitor II genes: enhancement of expression by sucrose. Plant Mol. Biol. 14, 527-536.
18. Kingston-Smith, A.H. and Pollock, C.J. (1996) Tissue level localization of acid invertase in leaves: an hypothesis for the regulation of carbon export. New Phytologist, 134, 423-432.
19. Koch, K.E. (1996) Carbohydrate-modulated gene expression in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 509-540.
20. Krapp, A. and Stitt, M. (1995) An evaluation of direct and indirect mechanisms for the 'sink-regulation' of photosynthesis in spinach: Changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold-girdling source leaves. Planta, 195, 313-323.
21. Krebbers, E., Seurinck, J., Herdies, L., Cashmore, A.R. and Timko, M.P. (1988) Four genes in two diverged subfamilies encode the ribulose-1,5-bisphosphate carboxylase small subunit polypeptides of Arabidopsis thaliana. Plant Mol. Biol. 11, 745-759.
22. Leutwiler, L.S., Meyerowitz, E.M. and Tobin, E.M. (1986) Structure and expression of three light-harvesting chlorophyll a/b-binding protein genes in Arabidopsis thaliana. Nucl. Acids Res. 14, 4051-4064.
23. Lichtenthaler, H.K. and Wellburn, A.R. (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc. Trans. 11, 591-592.
24. Lindner, R.C., Kirkpatrick, H.C. and Weeks, T.E. (1959) Some factors affecting the susceptibility of cucumber cotyledons to infection by tobacco mosaic virus. Phytopathology, 49, 78-88.
25. Loening, U.E. (1969) The determination of the molecular weight of ribonucleic acid by polyacrylamide-gel electrophoresis. The effects of changes in conformation. Biochem. J. 113, 131-138.
26. Long, D.E. and Cooke, R.C. (1974) Carbohydrate composition and metabolism of Senecio squalidus L leaves infected with Albugo tragopogonis (pers.) S. F. Gary. New Phytologist, 73, 889-899.
27. Mitchell, D.T., Fung, A.K. and Lewis, D.H. (1978) Changes in the ethanolsoluble carbohydrate composition and acid invertase in infected first leaf tissues susceptible to crown rust of oat and wheat stem rust. New Phytologist, 80, 381-392.
28. Pegg, G.F. (1981) The involvement of growth regulators in the diseased plant. In: Effects of Disease on the Physiology of Growing Plants (Ayres, P.G., ed.). Cambridge, UK: Cambridge University Press, pp. 149-177.
29. Ramloch-Lorenz, K., Knudsen, S. and Sturm, A. (1993) Molecular characterization of the gene for carrot cell wall β-fructosidase. Plant J. 4, 545-554.
30. Roberts, A.M. and Walters, D.R. (1988) Photosynthesis in discrete regions of leek leaves infected with the rust Puccinia allii Rud. New Phytologist, 110, 371-376.
31. Roberts, S.M. and Mitchell, D.T. (1979) Carbohydrate composition and invertase activity in poplar leaf tissues infected by Melampsorsa aecidioides (D.C.) Schroeter. New Phytologist, 83, 499-508.
32. Roitsch, T., Bittner, M. and Godt, D.E. (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.
33. Rolfe, S.A. and Scholes, J.D. (1995) Quantitative imaging of chlorophyll fluorescence. New Phytologist, 131, 69-79.
34. Ruban, A.V. and Horton, P. (1995) Regulation of non-photochemical quenching of chlorophyll fluorescence in plants. Aust. J. Plant Physiol. 22, 221-230.
35. Saettler, A.W. and Pound, G.S. (1966) Photosynthesis, carbohydrate levels, and translotion in radish leaves infected by Albugo Candida. Phytopathology, 56, 898.
36. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Extraction, purification, and analysis of messenger RNA from eukaryotic cells. In: Molecular cloning. A Laboratory Manual, 2nd edn. Cold Spring Harbor, USA: Cold Spring Harbor Laboratory Press.
37. Scholes, J.D. and Farrar, J.F. (1986) Increased rates of photosynthesis in localised regions of a barley leaf infected with brown rust. New Phytologist, 104, 601-612.
38. Scholes, J.D. and Farrar, J.F. (1987) Development of symptoms of brown rust of barley in relation to the distribution of fungal mycelium, starch accumulation and localized changes in the concentration of chlorophyll. New Phytologist, 107, 103-117.
39. Scholes, J.D. (1992) Photosynthesis: cellular and tissue aspects in diseased leaves. In: Pests and Pathogens (Ayres, P.G., ed.). Oxford, UK: BIOS Scientific Publishers Limited, pp. 85-105.
40. Scholes, J.D., Lee, P.J., Horton, P. and Lewis, D.H. (1994) Invertase: understanding changes in the photosynthetic and carbohydrate metabolism of barley leaves infected with powdery mildew. New Phytologist, 126, 213-222.
41. Scholes, J.D. and Rolfe, S.A. (1996) Photosynthesis in localised regions of oat leaves infected with crown rust (Puccinia coronata): quantitative imaging of chlorophyll fluorescence. Planta, 199, 573-582.
42. Sheen, J. (1994) Feedback control of gene expression. Photosynthesis Res. 39, 427-438.
43. Smeekens, S. and Rook, F. (1997) Sugar sensing and sugar-mediated signal transduction in plants. Plant Physiol. 115, 7-13.
44. Smeekens. S. (1998) Sugar regulation of gene expression in plants. Curr. Biol. 1, 230-234.
45. Stitt, M., von Schaewen, A. and Willmitzer, L. (1991) 'Sink' regulation of photosynthetic metabolism in transgenic tobacco plants expressing yeast invertase in their cell wall involves a decrease of the Calvin-cycle enzymes and an increase of glycolytic enzymes. Planta, 183, 40-50.
46. Sturm, A. and Chrispeels, M.J. (1990) cDNA cloning of carrot extracellular β-fructosidase and its expression in response to wounding and bacterial infection. Plant Cell, 2, 1107-1119.
47. Sturm, A., Sebková, V., Lorenz, K., Hardegger, M., Lienhard, S. and Unger, C. (1995) Development-and organ-specific expression of the genes for sucrose synthase and three isoenzymes of acid β-fructofuranosidase in carrot. Planta, 195, 601-610.
48. Tang, X., Rolfe, S.A. and Scholes, J.D. (1996) The effect of Albugo Candida (white blister rust) on the photosynthetic and carbohydrate metabolism of leaves of Arabidopsis thaliana. Plant, Cell Environ. 19, 967-975.
49. Von Schaewen, A., Stitt, M., Schmidt, R., Sonnewald, U. and Willmitzer, L. (1990) Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. EMBO J. 9, 3033-3044.
50. Weis, E., Meng, Q., Siebke, K., Wilmer, J. and Esfeld, P. (1998) Mapping metabolic differentiation in developing leaves by chlorophyll-a-fluorescence imaging. In: Proceedings of the 3rd Gatersleben Research Conference-Plant Metabolism and Development. IPK Gatersleben.
51. Whipps, J.M. and Cooke, R.C. (1978) Comparative physiology of Albugo tragopogonis-infected and Puccinia lagenophorae-infected plants of Senecio squalidus L. New Phytologist, 81, 307-319.
52. Whipps, J.M. and Lewis, D.H. (1981) Patterns of translocation, storage and interconversion of carbohydrates. In: Effects of Disease on the Physiology of Growing Plants (Ayres, P.G., ed.). Cambridge, UK: Cambridge University Press, pp. 47-83.
53. White, T.J., Bruns, T., Lee, S. and Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: a Guide to Methods and Applications (Innis, M.A., Gelfand, D.H., Sninsky J.J. and White T.J., eds). San Diego, CA: Academic Press, pp. 315-322.
54. Wright, D.P., Baldwin, B.C., Shephard, M.C and Scholes, J.D. (1995) Source-sink relationships in wheat leaves infected with powdery mildew. I. Alterations in carbohydrate metabolism. Physiol. Mol. Plant Pathol. 47, 237-253.
55. Wright, D.P., Scholes, J.D., Read, D.J. and Rolfe, S.A. (2000) Changes in carbon allocation and expression of carbon transporter genes in Betula pendula Roth. colonised by the ectomycorrhizal fungus Paxillus involutus (Batsch) Fr. Plant Cell Environment, 22, in press.
56. Zhang, L., Cohn, N.S. and Mitchell, J.P. (1996) Induction of a pea cell-wall invertase gene by wounding and its localized expression in phloem. Plant Physiol. 112, 1111-1117.
57. Zulu, J.N., Farrar, J.F. and Whitbread, R. (1991) Effects of phosphate supply on wheat seedlings infected with powdery mildew: carbohydrate metabolism of first leaves. New Phytologist, 118, 553-558.