Functional genomic approaches in cereal rusts

Canadian Journal of Plant Pathology

Volumn 34, Issue 1, 2012, Pages 3-12

  Bakkeren, Guus ^a   Song, Xiao ^a   Panwar, Vinay ^a   Linning, Rob ^a   Wang, Xiben ^a   Rampitsch, Christof ^a   McCallum, Brent ^a   Fellers, John ^b   Saville, Barry ^c  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b U S DEPARTMENT OF AGRICULTURE   (United States)

^c TRENT UNIVERSITY   (Canada)

Author keywords

avirulence; effector; P. graminis; P. striiformis; P. triticina; Puccinia species; secretome; wheat leaf rust

Indexed keywords

AGROBACTERIUM; FUNGI; PUCCINIA; PUCCINIA GRAMINIS; PUCCINIA STRIIFORMIS; PUCCINIA TRITICINA; RHIZOBIUM; TRITICUM AESTIVUM; UREDINALES;

EID: 84861405866     PISSN: 07060661     EISSN: 17152992     Source Type: Journal    
DOI: 10.1080/07060661.2012.664567     Document Type: Conference Paper

References (71)

1. ALI, S.,BAKKEREN, G. (2011). Fungal and oomycete effectors - strategies to subdue a host. Can. J. Plant Pathol., 33, 425-446.
2. BALDWIN, T.K., WINNENBURG, R., URBAN, M., RAWLINGS, C., KOEHLER, J.,HAMMOND-KOSACK, K.E. (2006). The pathogen-host interactions database (PHI-base) provides insights into generic and novel themes of pathogenicity. Mol. Plant-Microbe Interact., 19, 1451-1462.
3. BAXTER, L., TRIPATHY, S., ISHAQUE, N., BOOT, N., CABRAL, A., KEMEN, E., et al. (2010). Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science, 330, 1549-1551.
4. BRACHMANN, A., SCHIRAWSKI, J., MUELLER, 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.
5. BROEKER, K., BERNARD, F.,MOERSCHBACHER, B.M. (2006). An est library from Puccinia graminis f sp tritici reveals genes potentially involved in fungal differentiation. FEMS Microbiol. Lett., 256, 273-281.
6. CANTU, D., GOVINDARAJULU, M., KOZIK, A., WANG, M., CHEN, X., KOJIMA, K.K., et al. (2011). Next generation sequencing provides rapid access to the genome of Puccinia striiformis f sp tritici, the causal agent of wheat stripe rust. PLoS ONE, 6, e24230.
7. CATANZARITI, A.M., DODDS, P.N., LAWRENCE, G.J., AYLIFFE, M.A.,ELLIS, J.G. (2006). Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell, 18, 243-256.
8. CATANZARITI, A.-M., DODDS, P.N., VE, T., KOBE, B., ELLIS, J.G.,STASKAWICZ, B.J. (2010). The AvrM effector from flax rust has a structured C-terminal domain and interacts directly with the M resistance protein. Mol. Plant-Microbe Interact., 23, 49-57.
9. CERVANTES-CHÁVEZ, J.A., ALI, S.,BAKKEREN, G. (2011). Response to environmental stresses, cell-wall integrity, and virulence are orchestrated through the calcineurin pathway in Ustilago hordei. Mol. Plant- Microbe Interact., 24, 219-232.
10. CHOI, J., PARK, J., KIM, D., JUNG, K., KANG, S.,LEE, Y.H. (2010). Fungal secretome database: Integrated platform for annotation of fungal secretomes. BMC Genomics, 11, 105.
11. CHOQUER, M., FOURNIER, E., KUNZ, C., LEVIS, C., PRADIER, J.-M., SIMON, A., et al. (2007). Botrytis cinerea virulence factors: New insights into a necrotrophic and polyphagous pathogen. FEMS Microbiol. Lett., 277, 1-10.
12. CHUGH, A.,EUDES, F. (2008). Study of uptake of cell penetrating peptides and their cargoes in permeabilized wheat immature embryos. FEBS J., 275, 2403-2414.
13. DESVAUX, M., HÉBRAUD, M., TALON, R.,HENDERSON, I.R. (2009). Secretion and subcellular localizations of bacterial proteins: A semantic awareness issue. Trends Microbiol., 17, 139-145.
14. DONG, Y.-L., YIN, C.-T., HULBERT, S., CHEN, X.-M.,KANG, Z.-S. (2010). Cloning and expression analysis of three secreted protein genes from wheat stripe rust fungus Puccinia striiformis f sp tritici. World J. Microbiol. Biotechnol., 27, 1261-1265.
15. DRACATOS, P.M., DUMSDAY, J.L., OLLE, R.S., COGAN, N.O.I., DOBROWOLSKI, M.P., FUJIMORI, M., et al. (2006). Development and characterization of EST-SSR markers for the crown rust pathogen of ryegrass (Puccinia coronata f sp lolii). Genome, 49, 572-583.
16. DUPLESSIS, S., CUOMO, C.A., LIN, Y.-C., AERTS, A., TISSERANT, E., VENEAULT-FOURREY, C., et al. (2011). Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc. Natl. Acad. Sci. USA, 108, 9166-9171.
17. FEUILLET, C., LEACH, J.E., ROGERS, J., SCHNABLE, P.S.,EVERSOLE, K. (2011). Crop genome sequencing: lessons and rationales. Trends Plant Sci., 16, 77-88.
18. GLAWE, D.A. (2008). The powdery mildews: a review of the world's most familiar (yet poorly known) plant pathogens. Annu. Rev. Phytopathol., 46, 27-51.
19. GLAZEBROOK, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol., 43, 205-227.
20. GODFREY, D., BOHLENIUS, H., PEDERSEN, C., ZHANG, Z., EMMERSEN, J.,THORDAL-CHRISTENSEN, H. (2010). Powdery mildew and rust fungal effector candidates share N-terminal Y F/WxCmotif. BMC Genomics, 11, 317.
21. 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.
22. HIMMELBACH, A., ZIEROLD, U., HENSEL, G., RIECHEN, J., DOUCHKOV, D., SCHWEIZER, P., et al(2007). A set of modular binary vectors for transformation of cereals. Plant Physiol., 145, 1192-1200.
23. HOGENHOUT, S.A., VAN DER HOORN, R.A., TERAUCHI, R.,KAMOUN, S. (2009). Emerging concepts in effector biology of plantassociated organisms. Mol. Plant-Microbe Interact., 22, 115-122.
24. HOLUB, E.B.,COOPER, A. (2004). Matrix, reinvention in plants: how genetics is unveiling secrets of non-host disease resistance. Trends Plant Sci., 9, 211-214.
25. HOU, S., YANG, Y.,ZHOU, J.M. (2009). The multilevel and dynamic interplay between plant and pathogen. Plant Signal. Behav., 4, 283-293.
26. HU, G., KAMP, A., LINNING, R., NAIK, S.,BAKKEREN, G. (2007a). Complementation of Ustilago maydis MAPK mutants by a wheat leaf rust, Puccinia triticina homolog: potential for functional analyses of rust genes. Mol. Plant-Microbe Interact., 20, 637-647.
27. HU, G., LINNING, R., MCCALLUM, B., BANKS, T., CLOUTIER, S., BUTTERFIELD, Y., et al. (2007b). Generation of a wheat leaf rust, Puccinia triticina, EST database from stage-specific cDNA libraries. Mol. Plant Pathol., 8, 451-467.
28. 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.
29. JOLY, D., FEAU, N., TANGUAY, P.,HAMELIN, R. (2010). Comparative analysis of secreted protein evolution using expressed sequence tags from four poplar leaf rusts (Melampsora spp.). BMC Genomics, 11, 422.
30. JONES, J.D.G.,DANGL, J.L. (2006). The plant immune system. Nature, 444, 323-329.
31. KAMOUN, S. (2006). A catalogue of the effector secretome of plant pathogenic oomycetes. Annu. Rev. Phytopathol., 44, 41-60.
32. KORVES, T.,COLOSIMO, M.E. (2009). Controlled vocabularies for microbial virulence factors. Trends Microbiol., 17, 279-285.
33. KOSACK, K.E. (2006). The pathogen-host interactions database (PHI-base) provides insights into generic and novel themes of pathogenicity. Mol Plant-Microbe Interact., 19, 1451-1462.
34. KUCK, K.H.,REISENER, H.J. (1985). In vitro sporulation of race 32 of Puccinia graminis Pers. f sp tritici Erikss.,Henn. Physiol. Plant Pathol., 27, 259-268.
35. LAWRENCE, G.J., DODDS, P.N.,ELLIS, J.G. (2010). Transformation of the flax rust fungus, Melampsora lini: selection via silencing of an avirulence gene. Plant J., 61, 364-369.
36. LING, P.,WANG, M., CHEN, X.,CAMPBELL, K.G. (2007). Construction and characterization of a full-length cDNA library for the wheat stripe rust pathogen (Puccinia striiformis f sp tritici). BMC Genomics, 8, 145.
37. LINK, T.I.,VOEGELE, R.T. (2008). Secreted proteins of Uromyces fabae: similarities and stage specificity. Mol. Plant Pathol., 9, 59-66.
38. MA, J., HUANG, X., WANG, X., CHEN, X., QU, Z., HUANG, L., et al (2009). Identification of expressed genes during compatible interaction between stripe rust (Puccinia striiformis) and wheat using a cDNA library. BMC Genomics, 10, 586.
39. Manitoba Agriculture, Food Rural Initiatives, disease bulletin (http:// www.gov.mb.ca/agriculture/crops/diseases/fac43s00.html)
40. MAYORGA, M.E.,GOLD, S.E. (1999). A MAP kinase encoded by the ubc3 gene of Ustilago maydis is required for filamentous growth and full virulence. Mol. Microbiol., 34, 485-497.
41. MCCALLUM, B., MULOCK, B., SOMERS, D.J.,BAKKEREN, G. (2004). Inheritance of avirulence in the wheat leaf rust fungus Puccinia triticina. In Proceedings of the 11th International Cereal Rusts and Powdery Mildews Conference, Norwich, UK. Cereal Rusts and Powdery Mildews Bulletin 1.46.
42. MCCALLUM, B.D.,DEPAUW, R.M. (2008). A review of wheat cultivars grown in the Canadian prairies. Can. J. Plant Sci., 88, 649-677.
43. MCCALLUM, B.D., FETCH, T. Chong, J. (2007). Cereal rust control in Canada. Aust. J. Agric. Res., 58, 639-647.
44. MINDRINOS, M., KATAGIRI, F., YU, G.L.,AUSUBEL, F.M. (1994). The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell, 78, 1089-1099.
45. MUELLER, O., KAHMANN, R., AGUILAR, G., TREJO-AGUILAR, B., WU, A.,DE VRIES, R.P. (2008). The secretome of the maize pathogen Ustilago maydis. Fungal Genet. Biol., 45, S63-S70.
46. MULLER, P.,AICHINGER, C., FELDBRUGGE, M.,&KAHMANN, R. (1999). The MAP kinase kpp2 regulates mating and pathogenic development in Ustilago maydis. Mol. Microbiol, 34, 1007-1017.
47. NOWARA, D., GAY, A., LACOMME, C., SHAW, J., RIDOUT, C., DOUCHKOV, D., et al. (2010). HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell, 22, 3130-3141 Puccinia Group Sequencing Project, Broad Institute of Harvard and MIT (http://www.broadinstitute.org/
48. QI, X., DROSTE, T. Kao, C.C. (2011). Cell-penetrating peptides derived from viral capsid proteins. Mol. Plant-Microbe Interact., 24, 25-36.
49. RAFIQI, M., GAN, P.H.P., RAVENSDALE, M., LAWRENCE, G.J., ELLIS, J.G., JONES, D.A., et al. (2010). Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell, 22, 2017-2032.
50. RENTEL, M.C., LEONELLI, L., DAHLBECK, D., ZHAO, B.,STASKAWICZ, B.J. (2008). Recognition of the Hyaloperonospora parasitica effector ATR13 triggers resistance against oomycete, acterial, and viral pathogens. Proc. Natl. Acad. Sci. USA, 105, 1091-1096.
51. SAUNDERS, D.G.O., WIN, J., CANO, L.M., SZABO, L.J., KAMOUN, S.,RAFFAELE, S. (2012). Using hierarchical clustering of secreted protein families to classify and rank candidate effectors of rust fungi. PLoS ONE, 7, e29847.
52. SCHILLBERG, S., TIBURZY, R.,FISCHER, R. (2000). Transient transformation of the rust fungus Puccinia graminis f sp tritici. Mol. Gen. Genet., 262, 911-915.
53. SEIDL,M.F., VAN DEN ACKERVEKEN, G., GOVERS, F.,&SNEL, B. (2011). A domain-centric analysis of oomycete plant pathogen genomes reveals unique protein organization. Plant Physiol., 155, 628-644.
54. SODERLUND, C. (2009). Computational techniques for elucidating plant- pathogen interactions from large-scale experiments on fungi and oomycetes. Brief. Bioinform., 10, 654-663.
55. SONG, X., RAMPITSCH, C., SOLTANI, B., MAUTHE, W., LINNING, R., BANKS, T., et al. (2011). Proteome analysis of wheat leaf rust fungus, Puccinia triticina, infection structures enriched for haustoria. Proteomics, 11, 944-963.
56. STERGIOPOULOS, I.,DE WIT, P.J. (2009). Fungal effector proteins. Annu. Rev. Phytopathol., 47, 233-263.
57. THARA, V.K., FELLERS, J.P.,ZHOU, J.M. (2003). In planta induced genes of Puccinia triticina. Mol. Plant Pathol., 4, 51-56.
58. TORTO-ALALIBO, T., COLLMER, C.,GWINN-GIGLIO, M. (2009). The plant-associated microbe gene ontology (PAMGO) consortium: community development of new gene ontology terms describing biological processes involved in microbe-host interactions. BMC Microbiol., 9, S1.
59. VOEGELE, R.T.,MENDGEN, K. (2003). Rust haustoria: nutrient uptake and beyond. New Phytologist, 159, 93-100.
60. WEBB, C.A., SZABO, L.J., BAKKEREN, G., GARRY, C., STAPLES, R.C., EVERSMEYER, M., et al. (2006). Transient expression and insertional mutagenesis of Puccinia triticina using biolistics. Funct. Integr. Genomics, 6, 250-260.
61. WILLIAMS, P.G., SCOTT, K.J.,KUHL, J.L. (1966). Vegetative growth of Puccinia graminis f sp tritici in vitro. Phytopathology, 57, 1418-1419.
62. WILSON, R.A.,TALBOT, N.J. (2009). Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat. Rev. Microbiol., 7, 185-195.
63. WINNENBURG, R., BALDWIN, T.K., URBAN, M., RAWLINGS, C., KOHLER, J.,HAMMOND-KOSACK, K.E. (2006). PHI-base: A new database for pathogen host interactions. Nucl. Acids Res., 34, D459-464.
64. WINNENBURG, R., URBAN, M., BEACHAM, A., BALDWIN, T.K., HOLLAND, S., LINDEBERG, M., et al. (2008). PHI-base update: additions to the pathogen host interaction database. Nucl. Acids Res.,36, D572-576.
65. XU, J., LINNING, R., FELLERS, J., DICKINSON, M., ZHU, W., ANTONOV, I., et al. (2011). Gene discovery in EST sequences from the wheat leaf rust fungus Puccinia triticina sexual spores, asexual spores and haustoria, compared to other rust and corn smut fungi. BMC Genomics, 12, 161.
66. YIN, C., CHEN, X.,WANG, X., HAN, Q., KANG, Z.,&HULBERT, S. (2009). Generation and analysis of expression sequence tags from haustoria of the wheat stripe rust fungus Puccinia striiformis f sp tritici. BMC Genomics, 10, 626.
67. YIN, C.,HULBERT, S. (2011). Prospects for functional analysis of effectors from cereal rust fungi. Euphytica, 179, 57-67.
68. YIN, C., JURGENSON, J.E.,HULBERT, S.H. (2011). Development of a host-induced RNAi system in the wheat stripe rust fungus Puccinia striiformis f sp tritici. Mol. Plant-Microbe Interact., 24, 554-561.
69. ZHANG, L., MEAKIN, H.,DICKINSON, M. (2003). Isolation of genes expressed during compatible interactions between leaf rust (Puccinia triticina) and wheat using cDNA-AFLP. Mol. Plant Pathol., 4, 469-477.
70. ZHANG, Y., QU, Z., ZHENG, W., LIU, B., WANG, X., XUE, X., et al. (2008). Stage-specific gene expression during urediniospore germination in Puccinia striiformis f. sp tritici. BMC Genomics, 9, 203.
71. ZHONG, S., LENG, Y., FRIESEN, T.L., FARIS, J.D.,SZABO, L.J. (2009). Development and characterization of expressed sequence tag-derived microsatellite markers for the wheat stem rust fungus Puccinia graminis f sp tritici. Phytopathology, 99, 282-289.