Prospects for functional analysis of effectors from cereal rust fungi

Euphytica

Volumn 179, Issue 1, 2011, Pages 57-67

  Yin, Chuntao ^a   Hulbert, Scot ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Barley; Pseudomonas fluorescens; Pseudomonas syringae; RNAi; Type III secretion system; Wheat

Indexed keywords

AGROBACTERIUM; BACTERIA (MICROORGANISMS); DICOTYLEDONEAE; FUNGI; HORDEUM; POACEAE; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS SYRINGAE; PUCCINIA; PUCCINIA GRAMINIS; RHIZOBIUM; TRITICUM AESTIVUM; UREDINALES;

EID: 79953757420     PISSN: 00142336     EISSN: 15735060     Source Type: Journal    
DOI: 10.1007/s10681-010-0285-x     Document Type: Article

References (45)

1. Anderson DM, Fouts DE, Collmer A, Schneewind O (1999) Reciprocal secretion of proteins by the bacterial type III machines of plant and animal pathogens suggests universal recognition of mRNA targeting signals. Proc Natl Acad Sci USA 96: 12839-12843.
2. Ballance GM, Lamari L, Kowatsch R, and Bernier CC (1996) Cloning, expression and occurrence of the gene encoding the Ptr necrosis toxin from Pyrenophora tritici-repentis. Mol Plant Pathol http://www. bspp. org. uk/mppol/1996/1209ballance/.
3. Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P, Ilagan O, Johnson S, Plaetinck G, Munyikwa T, Pleau M, Vaughn T, Roberts J (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25: 1322-1326.
4. Block A, Li G, Fu AQ, Alfano JR (2008) Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol 11: 396-403.
5. Brueggeman R, Rostoks N, Kudrna D, Kilian A, Han F, Chen J, Druka A, Steffenson B, Kleinhofs A (2002) The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc Natl Acad Sci USA 99: 9328-9333.
6. Brueggeman R, Druka A, Nirmala J, Cavileer T, Drader T, Rostoks N, Mirlohi A, Bennypaul H, Gill U, Kudrna D, Whitelaw C, Kilian A, Han F, Sun Y, Gill K, Steffenson B, Kleinhofs A (2008) The stem rust resistance gene Rpg5 encodes a novel protein with nucleotide binding site, leucine-rich and protein kinase domains. Proc Natl Acad Sci USA 105: 14970-14975.
7. Catanzariti A-M, 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.
8. Chang JH, Urbach JM, Law TF, Arnold LW, Hu A, Gombar S, Grant SR, Ausubel FM, Dangl JL (2005) A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proc Natl Acad Sci USA 102: 2549-2554.
9. Chen XM, Line RF (1992) Inheritance of stripe rust resistance in wheat cultivars used to differentiate races of Puccinia striiformis in North America. Phytopathology 82: 633-637.
10. Chen XM, Line RF, Leung H (1995) Virulence and polymorphic DNA relationships of Pucciniastriiformis f. sp. hordei to other rusts. Phytopathology 85: 1335-1342.
11. Cloutier S, McCallum BD, Loutre C, Banks TW, Wicker T, Feuillet C, Keller B, Jordan MC (2007) Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Mol Biol 65: 93-106.
12. Collins N, Drake J, Ayliffe M, Sun Q, Ellis J, Hulbert S, Pryor T (1999) Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell 11: 1365-1376.
13. Currier H, Strugger S (1956) Aniline blue and fluorescence microscopy of callose in bulb scales of Allium cepa L. Protoplasma 45: 552-559.
14. DebRoy S, Thilmony R, Kwack YB, Nomura K, He SY (2004) A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc Natl Acad Sci U S A 101: 9927-9932.
15. Dodds PN, Lawrence GJ, Catanzariti A-M, Ayliffe M, Ellis J (2004) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16: 755-768.
16. Dodds PN, Lawrence GJ, Catanzariti A-M, Teh T, Ching I, Wang A, Ayliffe MA, Kobe B, Ellis JG (2006) Direct protein interaction underlies gene-for-gene specificity and co-evolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103: 8888-8893.
17. Ellis JG, Dodds PN, Lawrence GJ (2007) Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions. Annu Rev Phytopathol 45: 289-306.
18. Faris JD, Friesen TL (2009) Reevaluation of a tetraploid wheat population indicates that the Tsn1-ToxA interaction is the only factor governing Stagonospora nodorum blotch susceptibility. Phytopathology 99: 906-912.
19. Feuillet C, Travella S, Stein N, Albar L, Nublat A, Keller B (2003) Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proc Natl Acad Sci USA 100: 15253-15258.
20. Frizzi A, Huang S (2010) Tapping the silencing pathways for plant biotechnology. Plant Biotech J 8: 655-677.
21. Guttman DS, Greenberg JT (2001) Functional analysis of the type III effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringae with the use of a single-copy genomic integration system. Mol Plant Microbe Interact 14: 145-155.
22. Hahn M, Mendgen K (1992) Isolation by ConA binding of haustoria from different rust fungi and comparison of their surface qualities. Protoplasma 170: 95-103.
23. Ham JH, Bauer DW, Fouts DE, Collmer A (1998) A cloned Erwinia chrysanthemi Hrp (type III protein secretion) system functions in Escherichia coli to deliver Pseudomonas syringae Avr signals to plant cells and to secrete Avr proteins in culture. Proc Natl Acad Sci USA 95: 10206-10211.
24. Hogenhout SA, van der Hoorn RAL, Terauchi R, Kamoun S (2009) Emerging concepts in effector biology of plant-associated organisms. Mol Plant Microbe Interact 22: 115-122.
25. Huang L, Brooks SA, Li W, Fellers JP, Trick HN, Gill BS (2003) Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics 164: 655-664.
26. Huang G, Allen R, Davis EL, Baum TJ, Hussey RS (2006) Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc Natl Acad Sci USA 103: 14302-14306.
27. Jin Y, Szabo LJ, Carson M (2010) Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternate host. Phytopathology 100: 432-435.
28. Kvitko BH, Park DH, Vela′squez AC, Wei C-F, Russell AB et al (2009) Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 Type III secretion effector genes reveal functional overlap among effectors. PLoS Pathog 5(4): e1000388.
29. Lawrence GJ, Dodds PN, Ellis JG (2010) Transformation of the flax rust fungus, Melampsora lini: selection via silencing of an avirulence gene. Plant J 61: 364-369.
30. Manning VA, Ciuffetti LM (2005) Localization of Ptr ToxA produced by Pyrenophora tritici-repentis reveals protein import into wheat mesophyll cells. Plant Cell 17: 3203-3212.
31. Mudgett MB, Staskawicz BJ (1999) Characterization of the Pseudomonas syringae pv. tomato AvrRpt2 protein: demonstration of secretion and processing during bacterial pathogenesis. Mol Microbiol 32: 927-941.
32. Rentel MC, Leonelli L, Dahlbeck D, Zhao B, Staskawicz BJ (2008) Recognition of the Hyaloperonospora parasitica effector ATR13 triggers resistance against oomycete, bacterial, and viral pathogens. Proc Natl Acad Sci USA 105: 1091-1096.
33. Scofield SR, Huang L, Brandt AS, Gill BS (2005) Development of a virus induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiol 138: 2165-2173.
34. Sindhu AS, Maier TR, Mitchum MG, Hussey RS, Davis EL, Baum TJ (2009) Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success. J Exp Bot 60: 315-324.
35. Sohn KH, Lei R, Nemri A, Jones JD (2007) The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell 19: 4077-4090.
36. Thomas WJ, Thireault CA, Kimbrel JA, Chang JH (2009) Recombineering and stable integration of the Pseudomonas syringae pv. syringae 61 hrp/hrc cluster into the genome of the soil bacterium Pseudomonas fluorescens Pf0-1. Plant J 60: 919-928.
37. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11: 1187-1194.
38. Tuori RP, Wolpert TJ, Ciuffetti LM (2000) Heterologous expression of functional Ptr ToxA. Mol Plant Microbe Interact 13: 456-464.
39. Webb CA, Richter TE, Collins NC, Nicolas M, Trick HN, Pryor T, Hulbert SH (2003) Genetic and molecular characterizatio of the maize rp3 rust resistance locus. Genetics 169: 381-394.
40. Wellings C, Kandel K (2004) Pathogen dynamics associated with historic stripe (yellow) rust epidemics in Australia in 2002 and 2003. In: Proceedings of 11th In Cereal Rusts and Powdery Mildews Conf, Norwich, England, 22-27 August 2004, Cereal Rusts and Powdery Mildews Bulletin, Abstr A2. 74.
41. Yadav BC, Veluthambi K, Subramaniam K (2006) Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Mol Biochm Parasitol 148: 219-222.
42. Yin C, Chen X, Wang X, Han Q, Kang Z, Hulbert SH (2009) Generation and analysis of expression sequence tags from haustoria of the wheat stripe rust fungus Puccinia striiformis f. sp. tritici. BMC Genom 10: 626.
43. Zambino PJ, Kubelik AR, Szabo LJ (2000) Gene action and linkage of avirulence genes to DNA markers in the rust fungus Puccinia graminis. Phytopathology 90: 819-826.
44. Zhao B, Lin X, Poland J, Trick H, Leach J, Hulbert SH (2005) A maize resistance gene functions against bacterial streak disease in rice. Proc Natl Acad Sci USA 102: 15383-15388.
45. Zhou H, Li S, Deng Z, Wang X, Chen T, Zhang J, Chen S, Ling H, Zhang A, Wang D, Zhang X (2007) Molecular analysis of three new receptor-like kinase genes from hexaploid wheat and evidence for their participation in the wheat hypersensitive response to stripe rust fungus infection. Plant J 52: 420-434.