4 Fungal and Oomycete Biotrophy
Mark de Jong
Plant-Microbe Interactions, Department of Biology, Utrecht University, Padualaan 8, Utrecht, CH, 3584 The Netherlands
Present address: MicroArray Department, Swammerdam Institute for Life Sciences, University of Amsterdam, Kruislaan 318, 1098 SM, Amsterdam, The NetherlandsSearch for more papers by this authorGuido van den Ackerveken
Plant-Microbe Interactions, Department of Biology, Utrecht University, Padualaan 8, Utrecht, CH, 3584 The Netherlands
Search for more papers by this authorMark de Jong
Plant-Microbe Interactions, Department of Biology, Utrecht University, Padualaan 8, Utrecht, CH, 3584 The Netherlands
Present address: MicroArray Department, Swammerdam Institute for Life Sciences, University of Amsterdam, Kruislaan 318, 1098 SM, Amsterdam, The NetherlandsSearch for more papers by this authorGuido van den Ackerveken
Plant-Microbe Interactions, Department of Biology, Utrecht University, Padualaan 8, Utrecht, CH, 3584 The Netherlands
Search for more papers by this authorAbstract
Biotrophic fungal and oomycete pathogens have strikingly similar mechanisms to invade plants and retrieve nutrients. In particular, the obligate biotrophs form specialised feeding structures such as haustoria and intracellular hyphae that play an important role in host–pathogen signalling and nutrient retrieval. To establish a successful infection, pathogens need to overcome host defences, and suppression of plant defence responses is now a well-known phenomenon in disease. The molecular mechanisms of defence suppression by fungal and oomycete pathogens likely occurs via secreted or translocated effector proteins whose primary function is to establish compatibility. Many fungal and oomycete effector proteins are transported inside the host cell. In interactions with an obligate biotroph, the host provides the necessary nutrients for pathogen growth and reproduction. Specific transporters and metabolic enzymes in both host and pathogen contribute to nutrient exchange between the two organisms and hijacking of the host source–sink balance seems to be important for infection. Studies of plant–biotrophic fungal and plant–oomycete pathogen interactions, now exploiting a wealth of pathogen genome information, are providing unique insights into molecular mechanisms determining disease susceptibility and resistance.
References
- Allen, R.L., Bittner-Eddy, P.D., Grenville-Briggs, L.J., Meitz, J.C., Rehmany, A.P., Rose, L.E. and Beynon, J.L. (2004). Host–parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306, 1957–1960.
- Armstrong, M.R., Whisson, S.C., Pritchard, L., Bos, J.I., Venter, E., Avrova, A.O., et al. (2005). An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc. Natl. Acad. Sci. U.S.A. 102, 7766–7771.
- Bechinger, C. (1999). Optical measurements of invasive forces exerted by appressoria of a plant pathogenic fungus. Science 285, 1896–1899.
- Bhattacharjee, S., Hiller, N.L., Liolios, K., Win, J., Kanneganti, T.D., Young, C., et al. (2006). The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathog. 2, e50.
- Biemelt, S. and Sonnewald, U. (2006). Plant–microbe interactions to probe regulation of plant carbon metabolism. J. Plant Physiol. 163, 307–318.
- Bircher, U. and Hohl, H.R. (1997). Surface glycoproteins associated with appressoria formation and adhesion in Phytophthora palmivora . Mycol. Res. 101, 769–775.
- Bittner-Eddy, P.D., Allen, R.L., Rehmany, A.P., Birch, P. and Beynon, J.L. (2003). Use of suppression subtractive hybridization to identify downy mildew genes expressed during infection of Arabidopsis thaliana . Mol. Plant Pathol. 4, 501–507.
- Bos, J.I., Kanneganti, T.D., Young, C., Cakir, C., Huitema, E., Win, J., et al. (2006). The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana . Plant J. 48, 165–176.
- Both, M., Csukai, M., Stumpf, M.P. and Spanu, P.D. (2005). Gene expression profiles of Blumeria graminis indicate dynamic changes to primary metabolism during development of an obligate biotrophic pathogen. Plant Cell 17, 2107–2122.
- Buschges, R., Hollricher, K., Panstruga, R., Simons, G., Wolter, M., Frijters, A., et al. (1997). The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88, 695–705.
- Carzaniga, R., Bowyer, P. and O'Connel, R.J. (2001). Production of extracellular matrices during development of infection structures by the downy mildew pathogen Peronospora parasitica . New Phytol. 149, 83–93.
- Catanzariti, A.M., Dodds, P.N., Lawrence, G.J., Ayliffe, M.A. and Ellis, J.G. (2006). Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18, 243–256.
- Chisholm, S.T., Coaker, G., Day, B. and Staskawicz, B.J. (2006). Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803–814.
- Chou, H.-M., Bundock, M., 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.
- Clark, J.I.M. and Hall, J.L. (1998). Solute transport into healthy and powdery mildew-infected leaves of pea and uptake by powdery mildew mycelium. New Phytol. 140, 261–269.
- Consonni, C., Humphry, M.E., Hartmann, H.A., Livaja, M., Durner, J., Westphal, L., et al. (2006). Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat. Genet. 38, 716–720.
- Cutler, S.R., Ehrhardt, D.W., Griffitts, J.S. and Somerville, C.R. (2000). Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc. Natl. Acad. Sci. U.S.A. 97, 3718–3723.
- Dean, R.A. (1997). Signal pathways and appressorium morphogenesis. Annu. Rev. Phytopathol. 35, 211–234.
- Divon, H.H. and Fluhr, R. (2007). Nutrition acquisition strategies during fungal infection of plants. FEMS Microbiol. Lett. 266, 65–74.
- Dodds, P.N., Lawrence, G.J., Catanzariti, A.M., Ayliffe, M.A. and Ellis, J.G. (2004). The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16, 755–768.
- Feys, B.J., Wiermer, M., Bhat, R.A., Moisan, L.J., Medina-Escobar, N., Neu, C., et al. (2005). Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17, 2601–2613.
- Fotopoulos, V., Gilbert, M.J., Pittman, J.K., Marvier, A.C., Buchanan, A.J., Sauer, N., et al. (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.
- Freytag, S. and Mendgen, K. (1991). Carbohydrates on the surface of urediniospore- and basidiospore-derived infection structures of heteroecious and autoecious rust fungi. New Phytol. 119, 527–534.
- Gornhardt, B., Rouhara, I. and Schmelzer, E. (2000). Cyst germination proteins of the potato pathogen Phytophthora infestans share homology with human mucins. Mol. Plant Microbe. Interact. 13, 32–42.
- Haerter, A.C. and Voegele, R.T. (2004). A novel beta-glucosidase in Uromyces fabae: feast or fight? Curr. Genet. 45, 96–103.
- Hahn, M., Neef, U., Struck, C., Gottfert, M. and Mendgen, K. (1997). A putative amino acid transporter is specifically expressed in haustoria of the rust fungus Uromyces fabae . Mol. Plant Microbe. Interact. 10, 438–445.
- Harder, D.E. and Mendgen, K. (1982). Filipin-sterol complexes in bean rust– and oat crown rust–fungal/plant interactions: freeze-etch electron microscopy. Protoplasma 112, 46–54.
- Haritatos, E., Medville, R. and Turgeon, R. (2000). Minor vein structure and sugar transport in Arabidopsis thaliana . Planta 211, 105–111.
- Heisteruber, D., Schulte, P. and Moerschbacher, B.M. (1994). Soluble carbohydrate and invertase activity in stem rust-infected, resistant and susceptible near-isogenic wheat leaves. Physiol. Mol. Plant Pathol. 44, 111–123.
- Howard, R.J., Ferrari, M.A., Roach, D.H. and Money, N.P. (1991). Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc. Natl. Acad. Sci. U.S.A. 88, 11281–11284.
- Huckelhoven, R. (2005). Powdery mildew susceptibility and biotrophic infection strategies. FEMS Microbiol. Lett. 245, 9–17.
- Jakupovic, M., Heintz, M., Reichmann, P., Mendgen, K. and Hahn, M. (2006). Microarray analysis of expressed sequence tags from haustoria of the rust fungus Uromyces fabae . Fungal Genet. Biol. 43, 8–19.
- Jeon, J., Park, S.Y., Chi, M.H., Choi, J., Park, J., Rho, H.S., et al. (2007). Genome-wide functional analysis of pathogenicity genes in the rice blast fungus. Nat. Genet. 39, 561–565.
- Jia, Y., McAdams, S.A., Bryan, G.T., Hershey, H.P. and Valent, B. (2000). Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19, 4004–4014.
- Jones, J.D. and Dangl, J.L. (2006). The plant immune system. Nature 444, 323–329.
- Kamper, J., Kahmann, R., Bolker, M., Ma, L.J., Brefort, T., Saville, B.J., et al. (2006). Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis . Nature 444, 97–101.
- Kankanala, P., Czymmek, K. and Valent, B. (2007). Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19, 706–724.
- Kemen, E., Kemen, A.C., Rafiqi, M., Hempel, U., Mendgen, K., Hahn, M. and Voegele, R.T. (2005). Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol. Plant Microbe. Interact. 18, 1130–1139.
- Kistner, C., Winzer, T., Pitzschke, A., Mulder, L., Sato, S., Kaneko, T., et al. (2005). Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17, 2217–2229.
- Koh, S., Andre, A., Edwards, H., Ehrhardt, D. and Somerville, S. (2005). Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J. 44, 516–529.
- Kruger, J., Thomas, C.M., Golstein, C., Dixon, M.S., Smoker, M., Tang, S., et al. (2002). A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296, 744–747.
- Link, T., Lohaus, G., Heiser, I., Mendgen, K., Hahn, M. and Voegele, R.T. (2005). Characterization of a novel NADP(+)-dependent d-arabitol dehydrogenase from the plant pathogen Uromyces fabae . Biochem J. 389, 289–295.
- Lipka, V., Dittgen, J., Bednarek, P., Bhat, R., Wiermer, M., Stein, M., et al. (2005). Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis . Science 310, 1180–1183.
- Lipka, V. and Panstruga, R. (2005). Dynamic cellular responses in plant–microbe interactions. Curr. Opin. Plant. Biol. 8, 625–631.
- Lyngkjaer, M.F., Carver, T.L.W. and Zeyen, R.J. (2001). Virulent Blumeria graminis infection induces penetration susceptibility and suppresses race-specific hypersensitive resistance against avirulent attack in Mla1-barley. Physiol. Mol. Plant Pathol. 59, 243–256.
- Mackie, A.J., Roberts, A.M., Callow, J.A. and Green, J.R. (1993). Glycoproteins recognised by monoclonal antibodies UB7, UB8 and UB10 are expressed early in the development of pea powdery mildew haustoria. Physiol. Mol. Plant. Pathol. 43, 135–146.
- Mellersh, D. and Parniske, M. (2006). Common symbiosis genes of Lotus japonicus are not required for intracellular accommodation of the rust fungus Uromyces loti . New Phytol. 170, 641–644.
- Mendgen, K. and Deising, H. (1993). Infection structures of fungal plant pathogens – a cytological and physiological evaluation. New Phytol. 124, 193–213.
- Mendgen, K. and Hahn, M. (2002). Plant infection and the establishment of fungal biotrophy. Trends Plant Sci. 7, 352–356.
- Mendgen, K., Wirsel, S.G., Jux, A., Hoffmann, J. and Boland, W. (2006). Volatiles modulate the development of plant pathogenic rust fungi. Planta 224, 1353–1361.
-
Mims, C.W., Richardson, E.A., Holt III, B.F. and Dangl, J.L. (2004). Ultrastructure of the host-pathogen system in Arabidopsis thaliana leaves infected by the downy mildew Hyaloperonospora parasitica
. Can. J. Bot.
82, 1001–1008.
10.1139/b04-073 Google Scholar
- Murdoch, L.J., Kobayashi, I. and Hardham, A.R. (1998). Production and characterisation of monoclonal antibodies to cell wall components of the flax rust fungus. Eur. J. Plant Pathol. 104, 331–346.
- Nishimura, M.T., Stein, M., Hou, B.H., Vogel, J.P., Edwards, H. and Somerville, S.C. (2003). Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301, 969–972.
- O'Connell, R.J. (1987). Absence of a specialised interface between infection hyphae of Colletotrichum lindemuthianum and Phaseolus vulgaris . New Phytol. 107, 725–734.
- O'Connell, R.J., Pain, N.A., Hutchison, K.A., Jones, G.L. and Green, J.R. (1995). Ultrastructure and composition of the cell surfaces of infection structures formed by the fungal plant pathogen Colletotrichum lindemuthianum . J. Microsc. 181, 204–212.
- O'Connell, R.J. and Panstruga, R. (2006). Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol. 171, 699–718.
-
Ouchi, S., Oku, H., Hibino, C. and Akiyama, I. (1974). Induction of accessibility and resistance in leaves of barley by some races of Erysiphe graminis
. J. Phytopathol.
79, 24–34.
10.1111/j.1439-0434.1974.tb02686.x Google Scholar
- Panstruga, R. (2005). Serpentine plant MLO proteins as entry portals for powdery mildew fungi. Biochem. Soc. Transact. 33, 389–392.
- Perfect, S.E. and Green, J.R. (2001). Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol. Plant Pathol. 2, 101–108.
- Perfect, S.E., O'Connell, R.J., Green, E.F., Doering-Saad, C. and Green, J.R. (1998). Expression cloning of a fungal proline-rich glycoprotein specific to the biotrophic interface formed in the Colletotrichum–bean interaction. Plant. J. 15, 273–279.
- Pryce-Jones, E., Carver, T. and Gurr, S.J. (1999). The roles of cellulase enzymes and mechanical force in host penetration by Erysiphe graminis f.sp. hordei . Physiol. Mol. Plant Pathol. 55, 175–182.
- Rehmany, A.P., Gordon, A., Rose, L.E., Allen, R.L., Armstrong, M.R., Whisson, S.C., et al. (2005). Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17, 1839–1850.
- Richards, T.A., Dacks, J.B., Jenkinson, J.M., Thornton, C.R. and Talbot, N.J. (2006). Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr. Biol. 16, 1857–1864.
- Ridout, C.J., Skamnioti, P., Porritt, O., Sacristan, S., Jones, J.D. and Brown, J.K. (2006). Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 18, 2402–2414.
- Rooney, H.C., Van't Klooster, J.W., Van Der Hoorn, R.A., Joosten, M.H., Jones, J.D. and de Wit, P.J. (2005). Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308, 1783–1786.
- Sauer, N. (2007). Molecular physiology of higher plant sucrose transporters. FEBS Lett. 581, 2309–2317.
- Shan, W., Cao, M., Leung, D. and Tyler, B.M. (2004). The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Mol. Plant Microbe. Interact. 17, 394–403.
- Singh, U.S., Nashaat, N.I., Doughty, K.J. and Awasthi, R.P. (2002). Altered phenotypic response to Peronospora parasitica in Brassica juncea seedlings following prior inoculation with an avirulent or virulent isolate of Albugo candida . Eur. J. Plant Pathol. 108, 555–564.
- Sohn, J., Voegele, R.T., Mendgen, K. and 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.
- Sonnewald, U. and Willmitzer, L. (1992). Molecular approaches to sink–source interactions. Plant Physiol. 99, 1267–1270.
- Spanu, P.D. (2006). Why do some fungi give up their freedom and become obligate dependants on their host? New Phytol. 171, 447–450.
-
Spencer-Philips, P.T.N. (1997). Function of haustoria in epiphytic and endophytic infections. Adv. Bot. Res.
124, 309–333.
10.1016/S0065-2296(08)60077-4 Google Scholar
- Stadler, R., Lauterbach, C. and Sauer, N. (2005a). Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol. 139, 701–712.
- Stadler, R., Wright, K.M., Lauterbach, C., Amon, G., Gahrtz, M., Feuerstein, A., et al. (2005b). Expression of GFP-fusions in Arabidopsis companion cells reveals non-specific protein trafficking into sieve elements and identifies a novel post-phloem domain in roots. Plant J. 41, 319–331.
- Stark-Urnau, M. and Mendgen, K. (1995). Sequential deposition of plant glycoproteins and carbohydrates into the host-parasite interface of Uromyces vignae and Vigna sinesis . Evidence for endocytosis and secretion. Protoplasma 186, 1–11.
- Storr, T. and Hall, J.L. (1992). The effect of infection by Erysiphe pisi DC on acid and alkaline invertase activities and aspects of starch biochemistry in Pisum sativum L . New Phytol. 121, 535–543.
- Struck, C., Ernst, M. and Hahn, M. (2002). Characterization of a developmentally regulated amino acid transporter (AAT1p) of the rust fungus Uromyces fabae . Mol. Plant Pathol. 3, 23–30.
- Struck, C., Siebels, C., Rommel, O., Wernitz, M. and 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.
- Sutton, P.N., Gilbert, M.J., Williams, L.E. and Hall, J.L. (2007). Powdery mildew infection of wheat leaves changes host solute transport and invertase activity. Physiol. Plant. 129, 787–795.
- Sutton, P.N., Henry, M.J. and Hall, J.L. (1999). Glucose, and not sucrose, is transported from wheat to wheat powdery mildew. Planta 208, 426–430.
- Swarbrick, P.J., Schulze-Lefert, P. and Scholes, J.D. (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.
- Szabo, L.J. and Bushnell, W.R. (2001). Hidden robbers: the role of fungal haustoria in parasitism of plants. Proc. Natl. Acad. Sci. U.S.A. 98, 7654–7655.
- Takemoto, D., Jones, D.A. and Hardham, A.R. (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.
- Thomas, S.W., Rasmussen, S.W., Glaring, M.A., Rouster, J.A., Christiansen, S.K. and Oliver, R.P. (2001). Gene identification in the obligate fungal pathogen Blumeria graminis by expressed sequence tag analysis. Fungal. Genet. Biol. 33, 195–211.
- Thomma, B.P.H.J., Van Esse, H.P., Crous, P.W. and De Wit, P.J.G.M. (2005). Cladosporium fulvum (syn. Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae . Mol. Plant Pathol. 6, 379–393.
- Tian, M., Benedetti, B. and Kamoun, S. (2005). A Second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. Plant Physiol. 138, 1785–1793.
- Tian, M., Huitema, E., Da Cunha, L., Torto-Alalibo, T. and Kamoun, S. (2004). A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B. J. Biol. Chem. 279, 26370–26377.
- Tian, M., Win, J., Song, J., Van Der Hoorn, R., Van Der Knaap, E. and Kamoun, S. (2007). A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol. 143, 364–377.
- Tucker, S.L. and Talbot, N.J. (2001). Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu. Rev. Phytopathol. 39, 385–417.
- Tyler, B.M., Tripathy, S., Zhang, X., Dehal, P., Jiang, R.H., Aerts, A., et al. (2006). Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313, 1261–1266.
- Van Damme, M., Andel, A., Huibers, R.P., Panstruga, R., Weisbeek, P.J. and Van den Ackerveken, G. (2005). Identification of Arabidopsis loci required for susceptibility to the downy mildew pathogen Hyaloperonospora parasitica . Mol. Plant Microbe. Interact. 18, 583–592.
- Van Damme, M., Huibers, R.P., Elberse, J. and Van den Ackerveken, G. (2008). Arabidopsis DMR6 encodes a 2OG-Fe(II) oxygenase that is defense associated but required for susceptibility to downy mildew. Plant J. 54, 785–793.
- Van Den Burg, H.A., Harrison, S.J., Joosten, M.H., Vervoort, J. and de Wit, P.J. (2006). Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol. Plant Microbe. Interact 19, 1420–1430.
- Van Den Burg, H.A., Spronk, C.A., Boeren, S., Kennedy, M.A., Vissers, J.P., Vuister, G.W., et al. (2004). Binding of the AVR4 elicitor of Cladosporium fulvum to chitotriose units is facilitated by positive allosteric protein–protein interactions: the chitin-binding site of AVR4 represents a novel binding site on the folding scaffold shared between the invertebrate and the plant chitin-binding domain. J. Biol. Chem. 279, 16786–16796.
- Van Der Biezen, E.A., Juwana, H., Parker, J.E. and Jones, J.D. (2000). cDNA-AFLP display for the isolation of Peronospora parasitica genes expressed during infection in Arabidopsis thaliana . Mol. Plant Microbe. Interact. 13, 895–898.
- van Loon, L.C., Rep, M. and Pieterse, C.M. (2006). Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44, 135–162.
- 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.
- 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.
- Voegele, R.T., Wirsel, S., Moll, U., Lechner, M. and 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.
- Vogel, J. and Somerville, S. (2000). Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proc. Natl. Acad. Sci. U.S.A. 97, 1897–1902.
- Vogel, J.P., Raab, T.K., Schiff, C. and Somerville, S.C. (2002). PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis . Plant Cell 14, 2095–2106.
- Vogel, J.P., Raab, T.K., Somerville, C.R. and Somerville, S.C. (2004). Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition. Plant J. 40, 968–978.
- Weber, H., Borisjuk, L., Heim, U., Sauer, N. and Wobus, U. (1997). A role for sugar transporters during seed development: molecular characterization of a hexose and a sucrose carrier in fava bean seeds. Plant Cell 9, 895–908.
- Whisson, S.C., Boevink, P.C., Moleleki, L., Avrova, A.O., Morales, J.G., Gilroy, E.M., et al. (2007). A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450, 115–118.
- Win, J., Morgan, W., Bos, J., Krasileva, K.V., Cano, L.M., Chaparro-Garcia, A., et al. (2007). Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell 9, 2349–2369.
Citing Literature
Browse other articles of this reference work: