A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis

PLoS Biology

Volumn 8, Issue 2, 2010, Pages

  Wahl, Ramon ^a,b   Wippel, Kathrin ^c   Goos, Sarah ^a   Kämper, Jörg ^a,b   Sauer, Norbert ^c  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON 14; CARRIER PROTEIN; COMPLEMENTARY DNA; FRUCTOSE; GENOMIC DNA; GLUCOSE; MALTOSE; MONOSACCHARIDE; ORGANIC CARBON; RAFFINOSE; RNA; SUCROSE; TREHALOSE; TRITIUM; VIRULENCE FACTOR; FUNGAL PROTEIN; SUCROSE TRANSPORT PROTEIN, PLANT; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; CELL MEMBRANE; CORN; ESCHERICHIA COLI; FUNGAL VIRULENCE; FUNGUS; HYDROLYSIS; IMMUNE RESPONSE; ISOTOPE LABELING; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT FUNGUS INTERACTION; PLANT PATHOGEN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; USTILAGO MAYDIS; CONFOCAL MICROSCOPY; FLUORESCENCE MICROSCOPY; GENETIC COMPLEMENTATION; GENETICS; MAIZE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; POLYMERASE CHAIN REACTION; USTILAGO; VIRULENCE;

FUNGI; USTILAGO MAYDIS;

FUNGAL PROTEINS; GENETIC COMPLEMENTATION TEST; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; PHYLOGENY; PLANT DISEASES; PLANT PROTEINS; POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; SUCROSE; USTILAGO; VIRULENCE; ZEA MAYS;

EID: 77649092560     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000303     Document Type: Article

References (55)

1. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Rev Phytopathol 43: 205-227.
2. Kliebenstein DJ, Rowe HC (2008) Ecological costs of biotrophic versus necrotrophic pathogen resistance, the hypersensitive response and signal transduction. Plant Sci 174: 551-556.
3. Martinez-Espinoza AD, Garcia-Pedrajas MD, Gold SE (2002) The Ustilaginales as plant pest and model systems. Fungal Genet Biol 35: 1-20.
4. Mendgen K, Hahn M (2002) Plant infection and the establishment of fungal biotrophy. Trends Plant Sci 7: 352-356.
5. Bauer R, Oberwinkler F, Vánky K (1997) Ultrastructural markers and systematics in smut fungi and allied taxa. Can J Bot 75: 1273-1314.
6. Doehlemann G, Wahl R, Horst RJ, Voll LM, Usadel B, et al. (2008) Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J 56: 181-195.
7. Horst RJ, Engelsdorf T, Sonnewald U, Voll LM (2008) Infection of maize leaves with Ustilago maydis prevents establishment of C4 photosynthesis. J Plant Physiol 165: 19-28.
8. Schübler A, Martin H, Cohen D, Fritz M, Wipf D (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444: 933-936.
9. Polidori E, Ceccaroli P, Saltarelli R, Guescini M, Menotta M, et al. (2007) Hexose uptake in the plant symbiotic ascomycete Tuber borchii Vittadini: biochemical features and expression pattern of the transporter TBHXT1. Fungal Genet Biol 44: 187-198.
10. Voegele RT, Struck C, Hahn M, 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.
11. Scholes JD, Lee PJ, Horton P, Lewis DH (1994) Invertase: understanding changes in the photosynthetic and carbohydrate metabolism of barley leaves infected with powdery mildew. New Phytol 126: 213-222.
12. Tang X, Rolfe SA, Scholes JD (1996) The effect of Albugo candida (white blister rust) on the photosynthetic and carbohydrate metabolism of leaves of Arabidopsis. Plant Cell Environ 19: 967-975.
13. Herbers K, Meuwly P, Metraux JP, Sonnewald U (1996) Salicylic acidindependent induction of pathogenesis-related protein transcripts by sugars is dependent on leaf developmental stage. FEBS Lett 397: 239-244.
14. Ehness R, Ecker M, Godt DE, Roitsch T (1997) Glucose and stress independently regulate source and sink metabolism and defense mechanisms via signal transduction pathways involving protein phosphorylation. Plant Cell 9: 1825-1841.
15. Kocal N, Sonnewald U, Sonnewald S (2008) Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria. Plant Physiol 148: 1523-1536.
16. Schaarschmidt S, Kopka J, Ludwig-Müller J, Hause B (2007) Regulation of arbuscular mycorrhization by apoplastic invertases: enhanced invertase activity in the leaf apoplast affects the symbiotic interaction. Plant J 51: 390-405.
17. Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, et al. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97-101.
18. Sonnhammer ELL, von Heijne G, Krgh A (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. In: Glasgow J, ed. Proceedings of the sixth international conference of intelligent systems for molecular biology (ISMB98). Menlo Park (California): AAAI Press. pp 175-182.
19. Büttner M, Sauer S (2000) Monosaccharide transporters in plants: structure, function and physiology. Biochim Biophys Acta 1465: 263-274.
20. Cheng Q, Michels CA (1991) MAL11 and MAL61 encode the inducible highaffinity maltose transporter of Saccharomyces cerevisiae. J Bacteriol 173: 1817-1820.
21. Stambuk BU, da Silva MA, Panek AD, de Araujo PS (1999) Active alphaglucoside transport in Saccharomyces cerevisiae. FEMS Microbiol Lett 170: 105-110.
22. Alves SL Jr, Herberts RA, Hollatz C, Trichez D, Miletti LC, et al. (2008) Molecular analysis of maltotriose active transport and fermentation by Saccharomyces cerevisiae reveals a determinant role for the AGT1 permease. Appl Environ Microbiol 74: 1494-1501.
23. Viigand K, Tammus K, Alamäe T (2005) Clustering of MAL genes in Hansenula polymorpha: cloning of the maltose permease gene and expression from the divergent intergenic region between the maltose permease and maltase genes. FEMS Yeast Res 5: 1019-1028.
24. Reinders A, Ward JM (2001) Functional characterization of the alpha-glucoside transporter Sut1p from Schizosaccharomyces pombe, the first fungal homologue of plant sucrose transporters. Mol Microbiol 39: 445-454.
25. Wieczorke R, Krampe S, Weierstall T, Freidel K, Hollenberg CP, et al. (1999) Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae. FEBS Lett 464: 123-128.
26. Emr SD, Schekman R, Flessel MC, Thorner J (1983) An MF alpha 1-SUC2 (alpha-factor-invertase) gene fusion for study of protein localization and gene expression in yeast. Proc Natl Acad Sci U S A 80: 7080-7084.
27. Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Lett 521: 2309-2317.
28. Stambuk BU, Batista AS, Araujo PS (2000) Kinetics of active sucrose transport in Saccharomyces cerevisiae. J Biosci Bioenerget 89: 212-214.
29. M'Batchi B, Delrot S (1984) Parachloromercuribenzensulfonic acid. A potential tool for differential labeling of the sucrose transporter. Plant Physiol 70: 1436-1443.
30. Turgeon R, Gowan E (1990) Phloem loading in Coleus blumei in the absence of carrier-mediated uptake of export sugar from the apoplast. Plant Physiol 94: 1244-1249.
31. Preuss D, Mulholland J, Kaiser CA, Orlean P, Albright C, et al. (1991) Structure of the yeast endoplasmic reticulum: localization of ER proteins using immunofluorescence and immunoelectron microscopy. Yeast 7: 891-911.
32. Sauer N, Ludwig A, Knoblauch A, Rothe P, Gahrtz M, et al. (2004) AtSUC8 and AtSUC9 encode functional sucrose transporters, but the closely related AtSUC6 and AtSUC7 genes encode aberrant proteins in different Arabidopsis ecotypes. Plant J 40: 120-130.
33. Komor E, Haab D, Tanner W (1972) Unusual features of the active hexose uptake system of Chlorella vulgaris. Biochim Biophys Acta 266: 649-660.
34. Eddy AA (1982) Mechanisms of solute transport in selected eukaryotic microorganisms. Adv Microb Physiol 23: 1-78.
35. Nadwodnik J, Lohaus G (2008) Subcellular concentrations of sugar alcohols and sugars in relation to phloem translocation in Plantago major, Plantago maritima, Prunus persica, and Apium graveolens. Planta 227: 1079-1089.
36. Truernit E, Schmid J, Epple P, Illig J, Sauer N (2199) The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge. Plant Cell 8: 2169-2182.
37. Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ, et al. (2003) The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atbfruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol 132: 821-829.
38. Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9: 606-613.
39. Carpaneto A, Geiger D, Bamberg E, Sauer N, Fromm J, et al. (2005) Phloemlocalized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under the control of the sucrose gradient and the proton motive force. J Biol Chem 280: 21437-21443.
40. 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.
41. 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.
42. Heineke D, Sonnewald U, Büssis D, Günter G, Leidreiter K, et al. (1992) Apoplastic expression of yeast-derived invertase in potato: effects on photosynthesis, leaf solute composition, water relations, and tuber composition. Plant Physiol 100: 301-308.
43. Brachmann A, Weinzierl G, Kämper J, Kahmann R (2001) Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol Microbiol 42: 1047-1063.
44. Holliday R In: King RC, ed (1974) Handbook of genetics. Volume 1. New York (New York): Plenum Press. pp 575-595.
45. Gillissen B, Bergemann J, Sandmann C, Schroeer B, Bölker M, et al. (1992) A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell 68: 647-657.
46. Nikawa J, Tskagoshi Y, Yamashita S (1991) Isolation and characterization of two distinct myo-inositol transporter genes of Saccharomyces cerevisiae. J Biol Chem 266: 11184-11191.
47. Kämper J (2004) A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis. Mol Genet Genomics 271: 103-110.
48. Scherer M, Heimel K, Starke V, Kämper J (2006) The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis. Plant Cell 18: 2388-2401.
49. Aichinger C, Hansson K, Eichhorn H, Lessing F, Mannhaupt G, et al. (2003) Identification of plant-regulated genes in Ustilago maydis by enhancer-trapping mutagenesis. Mol Genet Genomics 270: 303-314.
50. Sambrook J, Frisch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Volumes 1 - 3. Cold Spring Harbor (New York): Cold Spring Harbor Laboratory Press.
51. Schulz B, Banuett F, Dahl M, Schlesinger R, Schäfer W, et al. (1990) The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60: 295-306.
52. Gietz D, St Jean A, Woods RA, Schiestl RH (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20: 1425.
53. Sauer N, Stolz J (1994) SUC1 and SUC2: two sucrose transporters from Arabidopsis thaliana; expression and characterization in baker's yeast and identification of the histidine-tagged protein. Plant J 6: 67-77.
54. Meyer S, Melzer M, Truernit E, Hümmer C, Besenbeck R, et al. (2000) AtSUC3, a gene encoding a new Arabidopsis sucrose transporter, is expressed in cells adjacent to the vascular tissue and in a carpel cell layer. Plant J 24: 869-882.
55. Brachmann A, Schirawski J, Müller P, Kahmann R (2003) An unusual MAP kinase is required for efficient penetration of the plant surface by Ustilago maydis. EMBO J 22: 2199-2210.