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Nutrient uptake in rust fungi: how sweet is parasitic life?

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Abstract

A better understanding of the fundamental principles of host-pathogen interactions should enable us to develop new strategies to control disease and to eliminate or at least manage their causative agents. This is especially true for obligate biotrophic parasites like the rust fungi. One vital aspect in the field of obligate biotrophic host-pathogen interactions is the mobilization, acquisition and metabolism of nutrients by the pathogen. This includes transporters necessary for the uptake of nutrients as well as enzymes necessary for their mobilization and metabolism. In a broader sense effector molecules reprogramming the host or triggering the infected cell into metabolic shifts favorable for the pathogen also play an important role in pathogen alimentation.

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References

  • Aked J, Hall JL (1993) The uptake of glucose, fructose and sucrose into pea powdery mildew (Erysiphe pisi DC) from the apoplast of pea leaves. New Phytol 123:277–282

    CAS  Google Scholar 

  • Ayres PG, Press MC, Spencer-Phillips PTN (1996) Effects of pathogens and parasitic plants on source–sink relationships. In: Zamski E, Schaffner AA (eds) Photoassimilate distribution in plants and crops—source sink relationships. Marcel Dekker Inc, New York, pp 479–499

    Google Scholar 

  • Bago B, Pfeffer PE, Douds DD Jr, Brouillette J, Becard G, Shachar-Hill Y (1999) Carbon metabolism in spores of the arbuscular mycorrhizal fungus Glomus intraradices as revealed by nuclear magnetic resonance spectroscopy. Plant Physiol 121:263–272

    PubMed  CAS  Google Scholar 

  • Baka ZA, Larous L, Losel DM (1995) Distribution of ATPase activity at the host–pathogen interfaces of rust infections. Physiol Mol Plant Pathol 47:67–82

    CAS  Google Scholar 

  • Basse CW, Bock K, Boller T (1992) Elicitors and suppressors of the defense response in tomato cells. Purification and characterization of glycopeptide elicitors and glycan suppressors generated by enzymatic cleavage of yeast invertase. J Biol Chem 267:10258–10265

    PubMed  CAS  Google Scholar 

  • Benhamou N, Grenier J, Chrispeels MJ (1991) Accumulation of ß-fructosidase in the cell walls of tomato roots following infection by a fungal wilt pathogen. Plant Physiol 97:739–750

    PubMed  CAS  Google Scholar 

  • Bhatia Y, Mishra S, Bisaria VS (2002) Microbial ß-glucosidases: cloning, properties, and applications. Crit Rev Biotechnol 22:375–407

    PubMed  CAS  Google Scholar 

  • Billett EE, Billett MA, Burnett JH (1977) Stimulation of maize invertase activity following infection by Ustilago maydis. Phytochemistry 16:1163–1166

    CAS  Google Scholar 

  • Boles E, Hollenberg CP (1997) The molecular genetics of hexose transport in yeasts. FEMS Microbiol Rev 21:85–111

    PubMed  CAS  Google Scholar 

  • Brown JK, Hovmøller MS (2002) Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537–541

    PubMed  CAS  Google Scholar 

  • Bushnell WR (1972) Physiology of fungal haustoria. Annu Rev Phytopathol 10:151–176

    Google Scholar 

  • Bushnell WR, Rowell JB (1981) Suppressors of defense reactions: a model for roles in specificity. Phytopathology 71:1012–1014

    Google Scholar 

  • Callow JA, Long DE, Lithgow ED (1980) Multiple molecular forms of invertase in maize smut Ustilago maydis infections. Physiol Plant Pathol 16:93–107

    CAS  Google Scholar 

  • Cantrill LC, Deverall BJ (1993) Isolation of haustoria from wheat leaves infected by the leaf rust fungus. Physiol Mol Plant Pathol 42:337–341

    Google Scholar 

  • Catanzariti AM, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG (2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18:243–256

    PubMed  CAS  Google Scholar 

  • Chaturvedi V, Wong B, Newman SL (1996) Oxidative killing of Cryptococcus neoformans by human neutrophils. Evidence that fungal mannitol protects by scavenging reactive oxygen intermediates. J Immunol 156:3836–3840

    PubMed  CAS  Google Scholar 

  • Chou HM, Bundock N, Rolfe SA, Scholes JD (2000) Infection of Arabidopsis thaliana leaves with Albugo candida (white blister rust) causes a reprogramming of host metabolism. Mol Plant Pathol 1:99–113

    PubMed  CAS  Google Scholar 

  • de Bary HA (1863) Recherches sur le developpement de quelques champignons parasites. Ann Sci Nat Part Bot 20:5–148

    Google Scholar 

  • Dodds PN, Lawrence GJ, Catanzariti AM, Ayliffe MA, Ellis JG (2004) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16:755–768

    PubMed  CAS  Google Scholar 

  • Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CI, Ayliffe MA, Kobe B, Ellis JG (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103:8888–8893

    PubMed  CAS  Google Scholar 

  • El Gueddari NE, Rauchhaus U, Moerschbacher BM, Deising HB (2002) Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi. New Phytol 156:103–112

    CAS  Google Scholar 

  • Eschrich W (1989) Phloem unloading of photoassimilates. In: Baker DA, Milburn JA (eds) Transport of photoassimilates. Longman Scientific & Technical, Harlow, UK, pp 206–263

    Google Scholar 

  • Fernandez MR, Heath MC (1991) Interactions of the nonhost French bean plant (Phaseolus vulgaris) parasitic and saprophytic fungi. IV. Effect of preinoculation with the bean rust fungus on growth of parasitic fungi nonpathogenic on beans. Can J Bot 69:1642–1646

    Google Scholar 

  • Flor HH (1955) Host-parasite interaction in flax rust—its genetics and other implications. Phytopathology 45:680–685

    Google Scholar 

  • Flor HH (1956) The complementary genetic systems in flax and flax rust. Adv Genet 8:29–54

    Google Scholar 

  • Freytag S, Mendgen K (1991a) Carbohydrates on the surface of urediniospore- and basidiospore-derived infection structures of heteroecious and autoecious rust fungi. New Phytol 119:527–534

    CAS  Google Scholar 

  • Freytag S, Mendgen K (1991b) Surface carbohydrates and cell wall structure of in vitro-induced uredospore infection structures of Uromyces viciae-fabae before and after treatment with enzymes and alkali. Protoplasma 161:94–103

    CAS  Google Scholar 

  • Gay JL, Salzberg A, Woods AM (1987) Dynamic experimental evidence for the plasma membrane ATPase domain hypothesis of haustorial transport and for ionic coupling of the haustorium of Erysiphe graminis to the host cell (Hordeum vulgare). New Phytol 107:541–548

    CAS  Google Scholar 

  • Gil F, Gay JL (1977) Ultrastructural and physiological properties of the host interfacial components of haustoria of Erysiphe pisi in vivo and in vitro. Physiol Plant Pathol 10:1–12

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Haerter AC, Voegele RT (2004) A novel ß-glucosidase in Uromyces fabae: feast or fight? Curr Genet 45:96–103

    PubMed  CAS  Google Scholar 

  • Hahn M, Mendgen K (1992) Isolation of ConA binding haustoria from different rust fungi and comparison of their surface qualities. Protoplasma 170:95–103

    CAS  Google Scholar 

  • Hahn M, Mendgen K (1997) Characterization of in planta-induced rust genes isolated from a haustorium-specific cDNA library. Mol Plant Microbe Interact 10:427–437

    PubMed  CAS  Google Scholar 

  • Hahn M, Deising H, Struck C, Mendgen K (1997a) Fungal morphogenesis and enzyme secretion during pathogenesis. In: Hartleb H, Heitefuss R, Hoppe H-H (eds) Resistance of crop plants against fungi. Gustav Fischer, Jena, pp 33–57

    Google Scholar 

  • Hahn M, Neef U, Struck C, Göttfert M, Mendgen K (1997b) A putative amino acid transporter is specifically expressed in haustoria of the rust fungus Uromyces fabae. Mol Plant Microbe Interact 10:438–445

    PubMed  CAS  Google Scholar 

  • Harder DE, Chong J (1984) Structure and physiology of haustoria. In: Bushnell WR, Roelfs AP (eds) The cereal rusts, vol I: origins, specificity, structure, and physiology. Academic Press Inc, Orlando, pp 431–476

    Google Scholar 

  • Harder DE, Chong J (1991) Rust haustoria. In: Mendgen K, Lesemann D-E (eds) Electron microscopy of plant pathogens. Springer, Berlin, pp 235–250

    Google Scholar 

  • Harder DE, Mendgen K (1982) Filipin-sterol complexes in bean rust- and oat crown rust-fungal/plant interactions: Freeze-etch electron microscopy Uromyces appendiculatus. Protoplasma 112:46–54

    Google Scholar 

  • Heath MC (1976) Ultrastructural and functional similarity of the haustorial neckband of rust fungi and the Casparian strip of vascular plants. Can J Bot 54:2484–2489

    Google Scholar 

  • Heath MC, Skalamera D (1997) Cellular interactions between plants and biotrophic fungal parasites. Adv Bot Res 24:195–225

    CAS  Google Scholar 

  • Heisterüber D, Schulte P, Moerschbacher BM (1994) Soluble carbohydrates and invertase activity in stem rust-infected, resistant and susceptible near-isogenic wheat leaves. Physiol Mol Plant Pathol 45:111–123

    Google Scholar 

  • Jakupovic M, Heintz M, Reichmann P, Mendgen K, Hahn M (2006) Microarray analysis of expressed sequence tags from haustoria of the rust fungus Uromyces fabae. Fungal Genet Biol 43:8–19

    PubMed  CAS  Google Scholar 

  • Jennings DH (1984) Polyol metabolism in fungi. Adv Microb Physiol 25:149–193

    PubMed  CAS  Google Scholar 

  • Jennings DB, Ehrenshaft M, Pharr DM, Williamson JD (1998) Roles for mannitol and mannitol dehydrogenase in active oxygen-mediated plant defense. Proc Natl Acad Sci USA 95:15129–15133

    PubMed  CAS  Google Scholar 

  • Jennings DB, Daub ME, Pharr DM, Williamson JD (2002) Constitutive expression of a celery mannitol dehydrogenase in tobacco enhances resistance to the mannitol-secreting fungal pathogen Alternaria alternata. Plant J 32:41–49

    PubMed  CAS  Google Scholar 

  • Kapooria RG, Mendgen K (1985) Infection structures and their surface changes during differentiation in Uromyces fabae. J Phytopathol 113:317–323

    Google Scholar 

  • Kemen A (2006a) RTP1p, eine neue Familie amyloid-ähnlicher Proteine. Dissertation, Universität Konstanz

  • Kemen E (2006b) Cytologie und Funktion eines amyloidähnlichen Proteins aus Rostpilzen. Dissertation, Universität Konstanz

  • Kemen E, Kemen AC, Rafiqi M, Hempel U, Mendgen K, Hahn M, Voegele RT (2005) Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol Plant Microbe Interact 18:1130–1139

    PubMed  CAS  Google Scholar 

  • Knogge W (1997) Elicitors and suppressors of the resistance response. In: Hartleb H, Heitefuss R, Hoppe H-H (eds) Resistance of crop plants against fungi. Gustav Fischer, Jena, pp 159–182

    Google Scholar 

  • Koh S, Andre A, Edwards H, Ehrhardt D, Somerville S (2005) Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J 44:516–529

    PubMed  CAS  Google Scholar 

  • Krishnan HB, Pueppke SG (1988) Invertases from rust-infected wheat leaves. J Plant Physiol 133:336–339

    CAS  Google Scholar 

  • Leah R, Kigel J, Svendsen I, Mundy J (1995) Biochemical and molecular characterization of a barley seed ß-glucosidase. J Biol Chem 270:15789–15797

    PubMed  CAS  Google Scholar 

  • Lee S, Eisenberg D (2003) Seeded conversion of recombinant prion protein to a disulfide-bonded oligomer by a reduction-oxidation process. Nat Struct Biol 10:725–730

    PubMed  CAS  Google Scholar 

  • Leon P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116

    PubMed  CAS  Google Scholar 

  • Lewis DH, Smith DC (1967) Sugar alcohols (polyols) in fungi and green plants. I. Distribution, physiology and metabolism. New Phytol 66:143–184

    CAS  Google Scholar 

  • Link T, Lohaus G, Heiser I, Mendgen K, Hahn M, Voegele RT (2005) Characterization of a novel NADP+-dependent d-arabitol dehydrogenase from the plant pathogen Uromyces fabae. Biochem J 389:289–295

    PubMed  CAS  Google Scholar 

  • Lohaus G, Pennewiss K, Sattelmacher B, Hussmann M, Hermann Mühling 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

    PubMed  CAS  Google Scholar 

  • Maclean DJ (1982) Axenic culture and metabolism of rust fungi. In: Scott KJ, Chakravorty AK (eds) The rust fungi. Academic Press, London, pp 37–120

    Google Scholar 

  • Maclean DJ, Scott KJ (1976) Identification of glucitol (sorbitol) and ribitol in a rust fungus, Puccinia graminis f. sp. tritici. J Gen Microbiol 97:83–89

    PubMed  CAS  Google Scholar 

  • Manners JM (1989) The host–haustorium interface in powdery mildews. Aust J Plant Physiol 16:45–52

    Google Scholar 

  • Manners JM, Gay JL (1982) Transport, translocation and metabolism of 14C-photosynthates at the host–parasite interface of Pisum sativum and Erysiphe pisi. New Phytol 91:221–244

    CAS  Google Scholar 

  • Manners JM, Maclean DJ, Scott KJ (1982) Pathways of glucose assimilation in Puccinia graminis. J Gen Microbiol 128:2621–2630

    CAS  Google Scholar 

  • Manners JM, Maclean DJ, Scott KJ (1984) Hexitols as major intermediates of glucose assimilation by mycelium of Puccinia graminis. Arch Microbiol 139:158–161

    CAS  Google Scholar 

  • Martin TJ, Ellingboe AH (1978) Genetic control of the 32P transfer from wheat to Erysiphe graminis f. sp. tritici during primary infection. Physiol Plant Pathol 13:1–11

    CAS  Google Scholar 

  • Mendgen K (1979) Microautoradiographic studies on host-parasite interactions. II. The exchange of 3H-lysine between Uromyces phaseoli and Phaseolus vulgaris. Arch Microbiol 123:129–135

    CAS  Google Scholar 

  • Mendgen K (1981) Nutrient uptake in rust fungi. Phytopathology 71:983–989

    CAS  Google Scholar 

  • Mendgen K, Hahn M (2002) Plant infection and the establishment of fungal biotrophy. Trends Plant Sci 7:352–356

    PubMed  CAS  Google Scholar 

  • Mendgen K, Nass P (1988) The activity of powdery-mildew haustoria after feeding the host cell with different sugars, as measured with a potentiometric cyanine dye. Planta 174:283–288

    CAS  Google Scholar 

  • Mendgen K, Struck C, Voegele RT, Hahn M (2000) Biotrophy and rust haustoria. Physiol Mol Plant Pathol 56:141–145

    Google Scholar 

  • Mims CW, Rodriguez-Lother C, Richardson EA (2002) Ultrastructure of the host–pathogen interface in daylily leaves infected by the rust fungus Puccinia hemerocallidis. Protoplasma 219:221–226

    PubMed  CAS  Google Scholar 

  • Moerschbacher BM, Mierau M, Graessner B, Noll U, Mort AJ (1999) Small oligomers of galacturonic acid are endogenous suppressors of disease resistance reactions in wheat leaves. J Exp Bot 50:605–612

    CAS  Google Scholar 

  • Myrbäck K (1960) Invertases. In: Boyer PD, Lardy H, Myrbäck K (eds) The enzymes, 2nd edn. Academic Press, New York, pp 379–396

    Google Scholar 

  • Nürnberger T, Brunner F (2002) Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr Opin Plant Biol 5:318–324

    PubMed  Google Scholar 

  • Parker JE (2003) Plant recognition of microbial patterns. Trends Plant Sci 8:245–247

    PubMed  CAS  Google Scholar 

  • Perfect SE, Green JR (2001) Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol Plant Pathol 2:101–108

    PubMed  CAS  Google Scholar 

  • Pfyffer G, Pfyffer BU, Rast DM (1986) The polyol pattern, chemotaxonomy, and phylogeny of the fungi. Sydowia 39:160–201

    Google Scholar 

  • Reisener HJ (1969) The metabolism of alanin, glycine and arginine in uredospores of Puccinia graminis var. tritici during germination. Arch Microbiol 69:101–113

    CAS  Google Scholar 

  • Ruffner HP, Geissmann M, Rast DM (1992) Plant and fungal invertases in grape berries infected with Botrytis cinerea. Physiol Mol Plant Pathol 40:181–189

    CAS  Google Scholar 

  • Ruiz E, Ruffner HP (2002) Immunodetection of Botrytis-specific invertase in infected grapes. J Phytopathol 150:76–85

    CAS  Google Scholar 

  • Shu P, Tanner KG, Ledingham GA (1954) Studies on the respiration of resting and germinating uredospores of wheat stem rust. Can J Bot 32:16–23

    CAS  Google Scholar 

  • Sohn J, Voegele RT, Mendgen K, Hahn M (2000) High level activation of vitamin B1 biosynthesis genes in haustoria of the rust fungus Uromyces fabae. Mol Plant Microbe Interact 13:629–636

    PubMed  CAS  Google Scholar 

  • Solomon PS, Tan K-C, Oliver RP (2003) The nutrient supply of pathogenic fungi; a fertile field for study. Mol Plant Pathol 4:203–210

    PubMed  Google Scholar 

  • Staples RC (2000) Research on the rust fungi during the twentieth century. Annu Rev Phytopathol 38:49–69

    PubMed  CAS  Google Scholar 

  • Staples RC (2001) Nutrients for a rust fungus: the role of haustoria. Trends Plant Sci 6:496–498

    PubMed  CAS  Google Scholar 

  • Stark-Urnau M, Mendgen K (1995) Sequential deposition of plant glycoproteins and polysaccharides at the host-parasite interface of Uromyces vignae and Vigna sinensis. Protoplasma 186:1–11

    CAS  Google Scholar 

  • Stoop JM, Mooibroek H (1998) Cloning and characterization of NADP-mannitol dehydrogenase cDNA from the button mushroom, Agaricus bi\orus, and its expression in response to NaCl stress. Appl Environ Microbiol 64:4689–4696

    PubMed  CAS  Google Scholar 

  • Struck C, Hahn M, Mendgen K (1996) Plasma membrane H+-ATPase activity in spores, germ tubes, and haustoria of the rust fungus Uromyces viciae-fabae. Fungal Genet Biol 20:30–35

    PubMed  CAS  Google Scholar 

  • Struck C, Siebels C, Rommel O, Wernitz M, Hahn M (1998) The plasma membrane H+-ATPase from the biotrophic rust fungus Uromyces fabae: molecular characterization of the gene (PMA1) and functional expression of the enzyme in yeast. Mol Plant Microbe Interact 11:458–465

    PubMed  CAS  Google Scholar 

  • Struck C, Ernst M, Hahn M (2002) Characterization of a developmentally regulated amino acid transporter (AAT1p) of the rust fungus Uromyces fabae. Mol Plant Pathol 3:23–30

    PubMed  CAS  Google Scholar 

  • Struck C, Müller E, Martin H, Lohaus G (2004) The Uromyces fabae UfAAT3 gene encodes a general amino acid permease that prefers uptake of in planta scarce amino acids. Mol Plant Pathol 5:183–189

    PubMed  CAS  Google Scholar 

  • Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121:1–8

    PubMed  CAS  Google Scholar 

  • Sturm A, Chrispeels MJ (1990) cDNA cloning of carrot extracellular ß-fructosidase and its expression in response to wounding and bacterial infection. Plant Cell 2:1107–1119

    PubMed  CAS  Google Scholar 

  • Sturm A, Tang GQ (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407

    PubMed  Google Scholar 

  • Sutton PN, Henry MJ, Hall JL (1999) Glucose, and not sucrose, is transported from wheat to wheat powdery mildew. Planta 208:426–430

    CAS  Google Scholar 

  • Szabo LJ, Bushnell WR (2001) Hidden robbers: the role of fungal haustoria in parasitism of plants. Proc Natl Acad Sci USA 98:7654–7655

    PubMed  CAS  Google Scholar 

  • 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 thaliana. Plant Cell Environ 19:967–975

    CAS  Google Scholar 

  • Tiburzy R, Martins EMF, Reisener HJ (1992) Isolation of haustoria of Puccinia graminis f. sp. tritici from wheat leaves. Exp Mycol 16:324–328

    Google Scholar 

  • Tymowska-Lalanne Z, Kreis M (1998) The plant invertases: physiology, biochemistry, and molecular biology. Adv Bot Res 28:71–117

    CAS  Google Scholar 

  • Voegele RT (2006) Uromyces fabae: development, metabolism, and interactions with its host Vicia faba. FEMS Microbiol Lett 259:165–173

    PubMed  CAS  Google Scholar 

  • Voegele RT, Mendgen K (2003) Rust haustoria: nutrient uptake and beyond. New Phytol 159:93–100

    CAS  Google Scholar 

  • 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 USA 98:8133–8138

    PubMed  CAS  Google Scholar 

  • Voegele RT, Hahn M, Lohaus G, Link T, Heiser I, Mendgen K (2005) Possible roles for mannitol and mannitol dehydrogenase in the biotrophic plant pathogen Uromyces fabae. Plant Physiol 137:190–198

    PubMed  CAS  Google Scholar 

  • Voegele RT, Wirsel S, 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

    PubMed  CAS  Google Scholar 

  • Voegele RT, Hahn M, Mendgen K (2009) The Uredinales: cytology, biochemistry, and molecular biology. In: Deising H (ed) The Mycota V Plant relationships, 2nd edn. Springer, Berlin, pp 79–94

    Google Scholar 

  • von Mohl H (1853) Ueber die Traubenkrankheit. Bot Z 11:585–590

    Google Scholar 

  • Weber H, Roitsch T (2000) Invertases and life beyond sucrose cleavage. Trends Plant Sci 5:47–48

    PubMed  CAS  Google Scholar 

  • Williams AM, Maclean DJ, Scott KJ (1984) Cellular location and properties of invertase in mycelium of Puccinia graminis. New Phytol 98:451–463

    CAS  Google Scholar 

  • Williams LE, Lemoine R, Sauer N (2000) Sugar transporters in higher plants—a diversity of roles and complex regulation. Trends Plant Sci 5:283–290

    PubMed  CAS  Google Scholar 

  • Wirsel SG, Voegele RT, Mendgen KW (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

    PubMed  CAS  Google Scholar 

  • Wright DP, Baldwin BC, Shephard MC, Scholes JD (1995) Source-sink relationships in wheat leaves infected with powdery mildew. I. Alterations in carbohydrate metabolism. Physiol Mol Plant Pathol 47:237–253

    CAS  Google Scholar 

  • Zhang Z, Henderson C, Perfect E, Carver TLW, Thomas BJ, Skamnioti P, Gurr SJ (2005) Of genes and genomes, needles and haystacks: Blumeria graminis and functionality. Mol Plant Pathol 6:561–575

    PubMed  CAS  Google Scholar 

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Acknowledgements

We are grateful to Annette Schmid, Christine Giele, and Heinz Vahlenkamp for technical assistance. Financial support for our work was provided by various grants provided by the Deutsche Forschungsgemeinschaft to RTV and KM.

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  1. Fachgebiet Phytopathologie, Institut für Phytomedizin, Fakultät Agrarwissenschaften, Universität Hohenheim, Otto-Sander-Straße 5, 70599, Stuttgart, Germany

    Ralf T. Voegele

  2. Lehrstuhl Phytopathologie, Fachbereich Biologie, Universität Konstanz, 78457, Konstanz, Germany

    Kurt W. Mendgen

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Voegele, R.T., Mendgen, K.W. Nutrient uptake in rust fungi: how sweet is parasitic life?. Euphytica 179, 41–55 (2011). https://doi.org/10.1007/s10681-011-0358-5

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