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

Molecular Plant-Microbe Interactions

Volumn 19, Issue 6, 2006, Pages 625-634

  Voegele, Ralf T ^a   Wirsel, Stefan ^b   Möll, Ulla ^a   Lechner, Melanie ^a   Mendgen, Kurt ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Sink marker

Indexed keywords

BETA FRUCTOFURANOSIDASE; FUNGAL PROTEIN; VEGETABLE PROTEIN;

ARTICLE; BASIDIOMYCETES; BIOLOGICAL MODEL; ENZYMOLOGY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYLOGENY; PICHIA; PLANT DISEASE; PLANT LEAF; SACCHAROMYCES CEREVISIAE; VICIA FABA;

BASIDIOMYCOTA; BETA-FRUCTOFURANOSIDASE; FUNGAL PROTEINS; MODELS, BIOLOGICAL; PHYLOGENY; PICHIA; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; SACCHAROMYCES CEREVISIAE; VICIA FABA;

EMBRYOPHYTA; FUNGI; PICHIA; SACCHAROMYCES CEREVISIAE; UREDINALES; UROMYCES VICIAE-FABAE; VICIA FABA;

EID: 33646875709     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-19-0625     Document Type: Article

References (55)

1. Alting-Mees, M. A., and Short, J. M. 1989. pBluescript II: Gene mapping vectors. Nucleic Acids Res. 17:9494.
2. Bendtsen, J. D., Nielsen, H., von Heijne, G., and Brunak, S. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
3. Benhamou, N., Grenier, J., and Chrispeels, M. J. 1991. Accumulation of beta-fructosidase in the cell walls of tomato roots following infection by a fungal wilt pathogen. Plant Physiol. 97:739-750.
4. Billett, E. E., Billett, M. A., and Burnett, J. H. 1977. Stimulation of maize invertase activity following infection by Ustilago maydis. Phytochemistry 16:1163-1166.
5. Boddy, L. M., Berges, T., Barreau, C., Vainstein, M. H., Dobson, M. J., Ballance, D. J., and Peberdy, J. F. 1993. Purification and characterisation of an Aspergillus niger invertase and its DNA sequence. Curr. Genet. 24:60-66.
6. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
7. Callow, J. A., Long, D. E., and Lithgow, E. D. 1980. Multiple molecular forms of invertase in maize smut Ustilago maydis infections. Physiol. Plant Pathol. 16:93-107.
8. Chou, H. M., Bundock, N., Rolfe, S. A., and Scholes, J. D. 2000. Infection of Arabidopsis thaliana leaves with Albugo Candida (white blister rust) causes a reprogramming of host metabolism. Mol. Plant Pathol. 1:99-113.
9. Deising, H., Jungblut, P. R., and Mendgen, K. 1991. Differentiation- related proteins of the broad bean rust fungus Uromyces viciae-fabae, as revealed by high resolution two-dimensional polyacrylamide gel electrophoresis. Arch. Microbiol. 155:191-198.
10. Elble, R. 1992. A simple and efficient procedure for transformation of yeasts. Biotechnology 13:18-20.
11. Emr, S. D., Schekman, R., Flessel, M. C., and Thorner, J. 1983. An MFα1-SUC2 (α-factor-invertase) gene fusion for study of protein localization and gene expression in yeast. Proc. Natl. Acad. Sci. U.S.A. 80:7080-7084.
12. 32P-based hybridizations. Anal. Biochem. 210:235-244.
13. Eschrich, W. 1989. Phloem unloading of photoassimilates. Pages 206-263 in: Transport of photoassimilates. D. A. Baker and J. A. Milburn, eds. Longman Scientific & Technical, Harlow, UK.
14. Fotopoulos, V., Gilbert, M. J., Pittman, J. K., Marvier, A. C., Buchanan, A. J., Sauer, N., Hall, J. L., and Williams, L. E. 2003. The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atβfruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol. 132:821-829.
15. 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.
16. Goetz, M., and Roitsch, T. 1999. The different pH optima and substrate specificities of extracellular and vacuolar invertases from plants are determined by a single amino- acid substitution. Plant J. 20:707-711.
17. Goetz, M., and Roitsch, T. 2000. Identification of amino acids essential for enzymatic activity of plant invertases. J. Plant Physiol. 157:581-585.
18. Haerter, A. C., and Voegele, R. T. 2004. A novel β-glucosidase in Uromyces fabae: Feast or fight? Curr. Genet. 45:96-103.
19. Hahn, M., and Mendgen, K. 1997. Characterization of in planta-induced rust genes isolated from a haustorium-specific cDNA library. Mol. Plant-Microbe Interact. 10:427-437.
20. 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. 45:111-123.
21. Heyer, A. G., Raap, M., Schroeer, B., Many, B., and Willmitzer, L. 2004. Cell wall invertase expression at the apical meristem alters floral, architectural, and reproductive traits in Arabidopsis thaliana. Plant J. 39:161-169.
22. Heyer, A. G., and Wendenburg, R. 2001. Gene cloning and functional characterization by heterologous expression of the fructosyltransferase of Aspergillus sydowi IAM 2544. Appl. Environ. Microbiol. 67:363-370.
23. Krishnan, H. B., and Pueppke, S. G. 1988. Invertases from rust-infected wheat leaves. J. Plant Physiol. 133:336-339.
24. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.) 227:680-685.
25. Livne, A., and Daly, J. M. 1966. Translocation in healthy and rust-affected beans. Phytopathology 56:170-175.
26. Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
27. Myrback, K. 1960. Invertases. Pages 379-396 in: The Enzymes. P. Boyer, H. Lardy, and K. Myrback, eds. Academic Press, New York.
28. Neumann, N. P., and Lampen, J. O. 1967. Purification and properties of yeast invertase. Biochemistry 6:468-475.
29. Perez, J. A., Rodriguez, J., Ruiz, T., and Rodriguez, L. 2001. Expression of Pichia anomala INVI gene in Saccharomyces cerevisiae results in two different active forms of hypoglycosylated invertase. Arch. Microbiol. 175:189-197.
30. Ramloch-Lorenz, K., Knudsen, S., and Sturm, A. 1993. Molecular characterization of the gene for carrot cell wall beta-fructosidase. Plant J. 4:545-554.
31. Rentsch, D., Laloi, M., Rouhara, I., Schmelzer, E., Delrot, S., and Frommer, W. B. 1995. NTR1 encodes a high affinity oligopeptide transporter in Arabidopsis. FEBS (Fed. Eur. Biol. Soc.) Lett. 370:264-268.
32. Roitsch, T., and Gonzalez, M. C. 2004. Function and regulation of plant invertases: Sweet sensations. Trends Plant Sci. 9:606-613.
33. Ruffner, H. P., Geissmann, M., and Rast, D. M. 1992. Plant and fungal invertases in grape berries infected with Botrytis cinerea. Physiol. Mol. Plant Pathol. 40:181-189.
34. Ruiz, E., and Ruffner, H. P. 2002. Immunodetection of Botrytis-specific invertase in infected grapes. J. Phytopathol. 150:76-85.
35. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
36. Scholes, J., Bundock, N., Wilde, R., and Rolfe, S. 1996. The impact of reduced vacuolar invertase activity on the photosynthetic and carbohydrate metabolism of tomato. Planta 200:265-272.
37. Sherman, F. 1991. Getting started with yeast. Pages 3-21 in: Methods in Enzymology: Guide to Yeast Genetics and Molecular Biology. C. Outline and G. R. Fink, eds. Academic Press, San Diego, CA, U.S.A.
38. Sohn, J., Voegele, R. T., Mendgen, K., and Hahn, M. 2000. High level activation of vitamin Bl biosynthesis genes in haustoria of the rust fungus Uromyces fabae. Mol. Plant-Microbe Interact. 13:629-636.
39. Studier, F. W., and Moffat, B. A. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:113-130.
40. Sturm, A. 1999. Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol. 121:1-8.
41. Sturm, A., and Tang, G. Q. 1999. The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci. 4:401-407.
42. Swofford, D. L. 2000. Phylogenetic Analysis Using Parsimony (* and Other Methods) Version 4. Sinauer Associates, Sunderland, MA, U.S.A.
43. 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.
44. Thrower, L. B., and Thrower, S. L. 1966. The effect of infection with Uromyces fabae on translocation in Broad Bean. Phytopathol. Z. 57:267-276.
45. Tymowska-Lalanne, Z., and Kreis, M. 1998. The plant invertases: Physiology, biochemistry, and molecular biology. Adv. Bot. Res. 28:71-117.
46. Voegele, R. T., Hahn, M., Lohaus, G., Link, T., Heiser, I., and Mendgen, K. 2005. Possible roles for mannitol and Mannitol Dehydrogenase in the biotrophic plant pathogen Uromyces fabae. Plant Physiol. 137:190-198.
47. Voegele, R. T., Struck, C., Hahn, M., and Mendgen, K. 2001. The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc. Natl. Acad. Sci. U.S.A. 98:8133-8138.
48. Weber, H., Borisjuk, L., Heim, U., Buchner, P., and Wobus, U. 1995. Seed coat-associated invertases of fava bean control both unloading and storage functions: Cloning of cDNAs and cell type-specific expression. Plant Cell 7:1835-1846.
49. Weber, H., and Roitsch, T. 2000. Invertases and life beyond sucrose cleavage. Trends Plant Sci. 5:47-48.
50. Weschke, W., Panitz, R., Gubatz, S., Wang, Q., Radchuk, R., Weber, H., and Wobus, U. 2003. The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. Plant J. 33:395-411.
51. Whipps, J. M., and Lewis, D. H. 1981. Patterns of translocation, storage and interconversion of carbohydrates. Pages 47-83 in: Effects of Disease on the Physiology of the Growing Plant. P. G. Ayers, ed, Cambridge University Press, Cambridge.
52. Williams, A. M., Maclean, D. J., and Scott, K. J. 1984. Cellular location and properties of invertase in mycelium of Puccinia graminis. New Phytol. 98:451-463.
53. Wirsel, S. G., Voegele, R. T., and Mendgen, K. W. 2001. Differential regulation of gene expression in the obligate biotrophic interaction of Uromyces fabae with its host Vicia faba. Mol. Plant-Microbe Interact. 14:1319-1326.
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. Yanai, K., Nakane, A., Kawate, A., and Hirayama, M. 2001. Molecular cloning and characterization of the fructooligosaccharide-producing beta-fructofuranosidase gene from Aspergillus niger ATCC 20611. Biosci. Biotechnol. Biochem. 65:766-773.