Abstract
The secretome of plant-associated fungi and oomycetes has been the subject of much research since the publication about 10 years ago of the first edition of “The Mycota: Plant Relationships”. The concept that filamentous microbes require secreted proteins to alter their environment and the organisms they colonize is not particularly novel, but technology has matured to the point where it is nowadays possible to generate catalogs of the complete set of secreted proteins (the secretome) for a given organism. This has been driven by the coming of age of genome sequencing coupled with robust computational predictions of secretion signals. This chapter surveys some of the key concepts and findings that recently emerged from the study of the fungal and oomycete secretome, with an emphasis on effector proteins.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Bhattacharjee S, Hiller NL, Liolios K, Win J, Kanneganti TD, Young C, Kamoun S, Haldar, K (2006) The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathog 2:e50
Birch PR, Rehmany AP, Pritchard L, Kamoun S, Beynon JL (2006) Trafficking arms: oomycete effectors enter host plant cells. Trends Microbiol 14:8-11
Bishop JG, Ripoll DR, Bashir S, Damasceno CM, Seeds JD, Rose JK (2004) Selection on Glycine beta-1,3- endoglucanase genes differentially inhibited by a Phytophthora glucanase inhibitor protein. Genetics 169:1009-1019
Bos JI, Kanneganti TD, Young C, Cakir C, Huitema E, Win, J, Armstrong MR, Birch PR, Kamoun S (2006) The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hyper- sensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant J 48:165-176
Catanzariti AM, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG (2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elici- tors. Plant Cell 18:243-256
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host- microbe interactions: shaping the evolution of the plant immune response. Cell 124:803-814
Dawkins R (1999) The extended phenotype: the long reach of the gene. Oxford University Press, Oxford 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
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 coevolu- tion of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103:8888-8893
Freitas-Junior LH, Bottius E, Pirrit LA, Deitsch KW, Scheidig C, Guinet F, Nehrbass U, Wellems TE, Scherf A (2000) Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407:1018-1022
Gout L, Fudal I, Kuhn ML, Blaise F, Eckert M, Cattolico L, Balesdent MH, Rouxel, T (2006) Lost in the middle of nowhere: the AvrLml avirulence gene of the Dothide- omycete Leptosphaeria maculans. Mol Microbiol 60:67-80
Haldar K, Kamoun S, Hiller NL, Bhattacharje S, van Ooij C (2006) Common infection strategies of pathogenic eukaryotes. Nat Rev Microbiol 4:922-931
Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T, Lopez-Estrano C, Haldar K (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306:1934-1937
Huitema E, Bos JIB, Tian M, Win J, Waugh ME, Kamoun S (2004) Linking sequence to phenotype in Phytophthora -plant interactions. Trends Microbiol 12:193-200
Jamir Y, Guo M, Oh HS, Petnicki-Ocwieja T, Chen S, Tang X, Dickman MB, Collmer A, Alfano JR (2004) Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant J 37:554-565
Janjusevic R, Abramovitch RB, Martin GB, Stebbins CE (2006) A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311:222-226
Jiang RH, Weide R, van de Vondervoort PJ, Govers F (2006) Amplification generates modular diversity at an avir- ulence locus in the pathogen Phytophthora. Genome Res 16:827-840
Joosten MHAJ, Vogelsang R, Cozijnsen TJ, Verberne MC, de Wit PJGM (1997) The biotrophic fungus Cladosporium fulvum circumvents Cf-4 mediated resistance by producing unstable AVR4 elicitors. Plant Cell 9:367-379
Kamoun S (2003) Molecular genetics of pathogenic oomycetes. Eukaryot Cell 2:191-199 Kamoun S (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol 44:41-60
Kamoun S (2007) Groovy times: filamentous pathogen effectors revealed. Curr Opin Plant Biol 10:358-365 Kanneganti T-D, Bai X, Tsai C-W, Win J, Meulia T, Goodin M, Kamoun S, Hogenhout SA (2007) A functional genetic assay for nuclear trafficking in plants. Plant J 50:149-158
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
Kruger J, Thomas CM, Golstein C, Dixon MS, Smoker M, Tang S, Mulder L, Jones JD (2002) A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296:744-747
Lahaye T, Bonas U (2001) Molecular secrets of bacterial type III effector proteins. Trends Plant Sci 6:479-485
Lee SJ, Kelley BS, Damasceno CM, St John B, Kim BS, Kim BD, Rose JK (2006) A functional screen to characterize the secretomes of eukaryotic pathogens and their hosts in planta. Mol Plant-Microbe Interact 19:1368-1377
Marti M, Good RT, Rug M, Knuepfer E, Cowman AF (2004) Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306:1930-1933
Menne KM, Hermjakob H, Apweiler R (2000) A comparison of signal sequence prediction methods using a test set of signal peptides. Bioinformatics l6:74l-742
Nielsen H, Brunak S, von Heijne G (l999) Machine learning approaches for the prediction of signal peptides and other protein sorting signals. Protein Eng l2:3-9 O'Connell RJ, Panstruga R (2006) Tete a tete inside a plant cell: establishing compatibility between plants and bio- trophic fungi and oomycetes. New Phytol l7l:699-7l8
Orbach MJ, Farrall L, Sweigard JA, Chumley FG, Valent B (2000) A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell l2:20l9-2032
Palma K, Zhang Y, Li X (2005) An importin alpha homolog, MOS6, plays an important role in plant innate immunity. Curr Biol l5:ll29-ll35
Panstruga R (2003) Establishing compatibility between plants and obligate biotrophic pathogens. Curr Opin Plant Biol 6:320-326
Rehmany AP, Gordon A, Rose LE, Allen RL, Armstrong MR, Whisson SC, Kamoun S, Tyler BM, Birch PR, Beynon JL (2005)
Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell l7:l839-l850
Rep M, van der Does HC, Meijer M, van Wijk R, Houterman PM, Dekker HL, de Koster CG, Cornelissen BJ (2004) A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Mol Microbiol 53:l373-l383
Ridout CJ, Skamnioti P, Porritt O, Sacristan S, Jones JD, Brown JK (2006) Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell l8:2402-24l4
Rooney HC, Van't Klooster JW, van der Hoorn RA, Joosten MH, Jones JD, de Wit PJ (2005) Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-de- pendent disease resistance. Science 308:l783-l786
Rose JK, Ham KS, Darvill AG, Albersheim P (2002) Molecular cloning and characterization of glucanase inhibitor proteins: coevolution of a counterdefense mechanism by plant pathogens. Plant Cell l4:l329-l345
Schneider G, Fechner U (2004) Advances in the prediction of protein targeting signals. Proteomics 4:l57l-l580
Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, Keller B, Seki H, Ulker B, Somssich IE, Schulze-Lefert P (2006) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 3l5:l098- ll03
Tian M, Huitema E, da Cunha L, Torto-Alalibo T, 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, Benedetti B, 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 l38:l785-l793
Tian M, Win J, Song J, van der Hoorn R, van der Knaap E, Kamoun S (2007) A Phytophthora infestans cystatin- like protein targets a novel tomato papain-like apo- plastic protease. Plant Physiol l43:364-377
Torto T, Li S, Styer A, Huitema E, Testa A, Gow NAR, van West P, Kamoun S (2003) EST mining and functional expression assays identify extracellular effector proteins from Phytophthora. Genome Res l3:l675-l685
Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RH, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL, Chapman J, Damasceno CM, Dorrance AE, Dou D, Dickerman AW, Dubchak IL, Garbelotto M, Gijzen M, Gordon SG, Govers F, Grunwald NJ, Huang W, Ivors KL, Jones RW, Kamoun S, Krampis K, Lamour KH, Lee MK, McDonald WH, Medina M, Meijer HJ, Nordberg EK, Maclean DJ, Ospina-Giraldo MD, Morris PF, Phuntumart V, Putnam NH, Rash S, Rose JK, Saki- hama Y, Salamov AA, Savidor A, Scheuring CF, Smith BM, Sobral BW, Terry A, Torto-Alalibo TA, Win J, Xu Z, Zhang H, Grigoriev IV, Rokhsar DS, Boore JL (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 3l3:l26l-l266
van den Burg HA, Spronk CA, Boeren S, Kennedy MA, Viss- ers JP, Vuister GW, de Wit PJ, Vervoort J (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:l6786-l6796
van den Burg HA, Harrison SJ, Joosten MH, Vervoort J, de Wit PJ (2006) Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant-Microbe Interact l9:l420-l430
van den Hooven HW, van den Burg HA, Vossen P, Boeren S, de Wit PJ, Vervoort J (200l) Disulfide bond structure of the AVR9 elicitor of the fungal tomato pathogen Cladosporium fulvum: evidence for a cystine knot. Biochemistry 40:3458-3466
van Kan JAL, van den Ackerveken GFJM, de Wit PJGM (l99l) Cloning and characterization of cDNA of avir- ulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. Mol Plant-Microbe Interact 4:52-59
Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong MR, Grouffaud S, van West P, Chapman S, Hein I, Toth IK, Pritchard L, Birch PR (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450:ll5-ll8
Win J, Morgan W, Bos J, Krasileva KV, Cano LM, Chaparro- Garcia A, Ammar R, Staskawicz BJ, Kamoun S (2007) Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic Oomycetes. Plant Cell l9:2349-2369
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Kamoun, S. (2009). The Secretome of Plant-Associated Fungi and Oomycetes. In: Deising, H.B. (eds) Plant Relationships. The Mycota, vol 5. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-87407-2_9
Download citation
DOI: https://doi.org/10.1007/978-3-540-87407-2_9
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-87406-5
Online ISBN: 978-3-540-87407-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)