Wheat gene TaS3 contributes to powdery mildew susceptibility

Plant Cell Reports

Volumn 32, Issue 12, 2013, Pages 1891-1901

  Li, Shaohui ^a   Ji, Rui ^a   Dudler, Robert ^b   Yong, Mingli ^a   Deng, Qide ^a   Wang, Zhengyi ^a   Hu, Dongwei ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Over expression; Powdery mildew; RNAi; Susceptibility gene; Wheat

Indexed keywords

ERYSIPHALES; TRITICUM AESTIVUM;

GREEN FLUORESCENT PROTEIN; MESSENGER RNA; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; ASCOMYCETES; CELL FRACTIONATION; CHEMISTRY; DISEASE PREDISPOSITION; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; PENETRANCE; PHYLOGENY; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; PROTEIN TRANSPORT; REPORTER GENE; WHEAT;

AMINO ACID SEQUENCE; ASCOMYCOTA; CLONING, MOLECULAR; DISEASE SUSCEPTIBILITY; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENES, REPORTER; GENETIC ASSOCIATION STUDIES; GREEN FLUORESCENT PROTEINS; MOLECULAR SEQUENCE DATA; PENETRANCE; PHYLOGENY; PLANT DISEASES; PLANT PROTEINS; PROTEIN TRANSPORT; RNA, MESSENGER; SUBCELLULAR FRACTIONS; TRITICUM;

EID: 84888041081     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-013-1501-7     Document Type: Article

References (96)

1. Aist JR, Bushnell WR (1991) Invasion of plant hosts by powdery mildew fungi and cellular mechanism of resistance. In: Cole GT, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Plenum Press, New York, pp 321-345.
2. Albar L, Bangratz-Reyser M, Hebrard E, Ndjiondjop MN, Jones M, Ghesquière A (2006) Mutations in the eIF (iso) 4G translation initiation factor confer high resistance of rice to Rice yellow mottle virus. Plant J 47: 417-426.
3. Baxter L, Tripathy S, Ishaque N et al (2010) Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330: 1549-1551.
4. Bhat RA, Miklis M, Schmelzer E, Schulze-Lefert P, Panstruga R (2005) Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc Natl Acad Sci USA 102: 3135-3140.
5. Burland TG (2000) DNASTAR's laser gene sequence analysis software. Methods Mol Biol 132: 71-91.
6. Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Töpsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88: 695-705.
7. Caldo RA, Nettleton D, Wise RP (2004) Interaction-dependent gene expression in Mla-specified response to barley powdery mildew. Plant Cell 16: 2514-2528.
8. Caldo RA, Nettleton D, Peng J, Wise RP (2006) Stage-specific suppression of basal defense discriminates barley plants containing fast- and delayed-acting Mla powdery mildew resistance alleles. Mol Plant Microbe Interact 19: 939-947.
9. Christensen AH, Sharrock RA, Quail PH (1992) Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 18: 675-689.
10. Diaz-Pendon JA, Truniger V, Nieto C, Garcia-Mas J, Bendahmane A, Aranda MA (2004) Advances in understanding recessive resistance to plant viruses. Mol Plant Pathol 5: 223-233.
11. Dong WB, Nowara D, Schweizer P (2006) Protein polyubiquitination plays a role in basal host resistance of barley. Plant Cell 18: 3321-3331.
12. Douchkov D, Nowara D, Zierold U, Schweizer P (2005) A high-throughput gene-silencing system for the functional assessment of defense-related genes in barley epidermal cells. Mol Plant Microbe Interact 18: 755-761.
13. Duplessis S, Cuomo CA, Lin YC et al (2011) Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci USA 108: 9166-9171.
14. Eckardt NA (2002) In this issue: plant disease susceptibility genes? Plant Cell 14: 1983-1986.
15. Eckey C, Korell M, Leib K, Biedenkopf D, Jansen C, Langen G, Kogel KH (2004) Identification of powdery mildew-induced barley genes by cDNA-AFLP: functional assessment of an early expressed map kinase. Plant Mol Biol 55: 1-15.
16. Eichmann R, Bischof M, Weis C, Shaw J, Lacomme C, Schweizer P, Duchkov D, Hensel G, Kumlehn J, Hückelhoven R (2010) BAX INHIBITOR-1 is required for full susceptibility of barley to powdery mildew. Mol Plant Microbe Interact 23: 1217-1227.
17. Elmore ZC, Donaher M, Matson BC, Murphy H, Westerbeck JW, Kerscher O (2011) Sumo-dependent substrate targeting of the SUMO protease Ulp1. BMC Biol. doi: 10. 1186/1741-7007-9-74.
18. Frye CA, Innes RW (1998) An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell 10: 947-956.
19. Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci USA 98: 373-378.
20. Fung RW, Gonzalo M, Fekete C, Kovacs LG, He Y, Marsh E, McIntyre LM, Schachtman DP, Qiu W (2008) Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol 146: 236-249.
21. Green JR, Carver TLW, Gurr SJ (2002) The formation and function of infection and feeding structures. In: Belanger RR, Bushnell WR, Dik AJ, Carver TLW (eds) The powdery mildews: a comprehensive treatise. American Phytopathological Society (APS) Press, St. Paul, pp 66-82.
22. Hanania U, Furman-Matarasso N, Ron M, Avni A (1999) Isolation of a novel SUMO protein from tomato that suppresses EIX-induced cell death. Plant J 19: 533-541.
23. Hardham AR, Jones DA, Takemoto D (2007) Cytoskeleton and cell wall function in penetration resistance. Curr Opin Plant Biol 10: 342-348.
24. Hickey CM, Wilson NR, Hochstrasser M (2012) Function and regulation of SUMO proteases. Mol Cell Biol 13: 755-766.
25. Hoefle C, Loehrer M, Schaffrath U, Frank M, Schultheiss H, Hückelhoven R (2009) Transgenic suppression of cell death limits penetration success of the soybean rust fungus Phakopsora pachyrhizi into epidermal cells of barley. Phytopathology 99: 220-226.
26. Hoefle C, Huesmann C, Schultheiss H, Börnke F, Hensel G, Kumlehn J, Hückelhoven R (2011) A barley ROP GTPase ACTIVATING PROTEIN associates with microtubules and regulates entry of the barley powdery mildew fungus into leaf epidermal cells. Plant Cell 23: 2422-2439.
27. Hotson A, Mudgett MB (2004) Cysteine proteases in phytopathogenic bacteria: identification of plant targets and activation of innate immunity. Curr Opin Plant Biol 7: 384-390.
28. Hotson A, Chosed R, Shu H, Orth K, Mudgett MB (2003) Xanthomonas type III efector XopD targets SUMO-conjugated proteins in planta. Mol Microbiol 50: 377-389.
29. Hu DW, Li ZQ, Kang ZS (1997) Cytological studies on development and primary infection of Erysiphe graminis f. sp. tritici in wheat. Acta Univ Agric Boreali Occidentalia 25: 1-7.
30. Huang X, Wang G, Shen YZ, Huang ZJ (2012) The wheat gene TaST can increase the salt tolerance of transgenic Arabidopsis. Plant Cell Rep 31: 339-347.
31. Huang CJ, Hu GJ, Li FF, Li YQ, Wu JX, Zhou XP (2013) NbPHAN, a MYB transcriptional factor, regulates leaf development and affects drought tolerance in Nicotiana benthamiana. Physiol plantarum. doi: 10. 1111/ppl. 12031.
32. Hückelhoven R (2005) Powdery mildew susceptibility and biotrophic infection strategies. FEMS Microbiol Lett 245: 9-17.
33. Hückelhoven R, Panstruga R (2011) Cell biology of the plant-powdery mildew interaction. Curr Opin Plant Biol 14: 738-746.
34. Hückelhoven R, Dechert C, Kogel KH (2003) Overexpression of barley BAX inhibitor 1 induces breakdown of mlo mediated penetration resistance to Blumeria graminis. Proc Natl Acad Sci USA 100: 5555-5560.
35. Humphry M, Consonni C, Panstruga R (2006) Mlo-based powdery mildew immunity: silver bullet or simply nonhost resistance? Mol Plant Pathol 7: 605-610.
36. Jørgensen JH (1992) Discovery, characterization and exploitation of mlo powdery mildew resistance in barley. Euphytica 63: 141-152.
37. Jørgensen JH (1994) Genetics of powdery mildew resistance in barley. Plant Sci 13: 97-119.
38. Kang BC, Yeam I, Frantz JD, Murphy JF, Jahn MM (2005) The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J 42: 392-405.
39. Kemen E, Jones JDG (2012) Obligate biotroph parasitism: can we link genomes to lifestyles? Trends Plant Sci 17: 448-457.
40. Kemen E, Gardiner A, Schultz-Larsen T, Kemen AC, Balmuth AL, Robert-Seilaniantz A, Bailey K, Holub E, Studholme DJ, MacLean D, Jones JDG (2011) Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biol 9: 1-21.
41. Kim J, Taylor KW, Hotson A, Keegan M, Schmelz EA, Mudgett MB (2008) XopD SUMO protease affects host transcription, promotes pathogen growth, and delays symptom development in Xanthomonas-infected tomato leaves. Plant Cell 20: 1915-1929.
42. Kristensen BK, Ammitzboll H, Rasmussen SK, Nielsen KA (2001) Transient expression of a vacuolar peroxidase increases susceptibility of epidermal barley cells to powdery mildew. Mol Plant Pathol 2: 311-317.
43. Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Sung DY, Vierstra RD (2003) The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and -2 conjugates is increased by stress. J Biol Chem 278: 6862-6872.
44. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2. 0. Bioinformatics 23: 2947-2948.
45. Leath S, Heun M (1990) Identification of powdery mildew resistance genes in cultivars of soft red winter wheat. Plant Dis 74: 747-752.
46. Li SJ, Hochstrasser M (1999) A new protease required for cell-cycle progression in yeast. Nature 398: 246-251.
47. Lipka U, Fuchs R, Lipka V (2008) Arabidopsis non-host resistance to powdery mildews. Curr Opin Plant Biol 11: 404-411.
48. -ΔΔCT method. Methods 25: 402-408.
49. Lois LM, Lima CD, Chua NH (2003) Small ubiquitin-like modifier modulates abscisic acid signaling in Arabidopsis. Plant Cell 15: 1347-1359.
50. Lyngkjaer MF, Newton AC, Atzema JL, Baker SJ (2000) The barley mlo-gene: an important powdery mildew resistance source. Agronomie 20: 745-756.
51. Martin K, Kopperud K, Chakrabarty R, Banerjee R, Brooks R, Goodin MM (2009) Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. Plant J 59: 150-162.
52. Meijer LK, Schesser K, Wolf-Watz H, Sassone-Corsi P, Pettersson S (2000) The bacterial protein YopJ abrogates multiple signal transduction pathways that converge on the transcription factor CREB. Cell Microbiol 2: 231-238.
53. Melchoir F (2000) SUMO-nonclassical ubiquitin. Annu Rev Cell Dev Biol 16: 591-626.
54. Mossessova E, Lima CD (2000) Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol Cells 5: 865-876.
55. Murtas G, Reeves PH, Fu YF, Bancroft I, Dean C, Coupland G (2003) A nuclear protease required for flowering-time regulation in Arabidopsis reduces the abundance of small ubiquitinrelated modifier conjugates. Plant Cell 15: 2308-2319.
56. Mysore KS, Crasta OR, Tuori RP, Folkerts O, Swirsky PB, Martin GB (2002) Comprehensive transcript profiling of Pto- and Prf-mediated host defense response to infection by Pseudomonas syringae pv. tomato. Plant J 32: 299-315.
57. Nicaise V, German-Retana S, Sanjuan R, Dubrana MP, Mazier M, Maisonneuve B, Candresse T, Caranta C, LeGall O (2003) The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the Potyvirus Lettuce mosaic virus. Plant Physiol 132: 1272-1282.
58. Nieto C, Morales M, Orjeda G, Clepet C, Monfort A, Sturbois B, Puigdomènech P, Pitrat M, Caboche M, Dogimont C, Garcia-Mas J, Aranda MA, Bendahmane A (2006) An eIF4E allele confers resistance to an uncapped and nonpolyadenylated RNA virus in melon. Plant J 48: 452-462.
59. Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301: 969-972.
60. Noel L, Thieme F, Nennstiel D, Bonas U (2002) Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island. J Bacteriol 184: 1340-1348.
61. O'Connell JR, Panstruga R (2006) Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol 171: 699-718.
62. Orth K (2002) Function of the yersinia effector YopJ. Curr Opin Microbiol 5: 38-43.
63. Orth K, Xu ZH, Mudgett MB, Bao ZQ, Palmer LE, Bliska JB, Mangel WF, Staskawicz B, Dixon JE (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290: 1594-1597.
64. Panstruga R (2003) Establishing compatibility between plants and obligate biotrophic pathogens. Curr Opin Plant Biol 6: 320-326.
65. Panstruga R (2005) Serpentine plant mlo proteins as entry portals for powdery mildew fungi. Biochem Soc Trans 33: 389-392.
66. Panwar V, McCallum B, Bakkeren G (2013) Endogenous silencing of Puccinia triticina pathogenicity genes through in planta-expressed sequences leads to the suppression of rust diseases on wheat. Plant J 73: 521-532.
67. Park HJ, Kim WY, Park HC, Lee SY, Bohnert HJ, Yun DJ (2011) SUMO and SUMOylation in plants. Mol Cells 32: 305-316.
68. Pavan S, Jacobsen E, Visser RGF, Bai YL (2010) Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol Breed 25: 1-12.
69. Piffanelli P, Ramsay L, Waugh R, Benabdelmouna A, D'Hont A, Hollricher K, Jørgensen JH, Paul Schulze-Lefert P, Panstruga R (2004) A barley cultivation-associated polymorphism conveys resistance to powdery mildew. Nature 430: 887-891.
70. Raffaele S, Farrer RA, Cano LM, Studholme DJ, MacLean D, Thines M, Jiang RHY, Zody MC, Kunjeti SG, Donofrio NM, Meyers BC, Nusbaum C, Kamoun C (2010) Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330: 1540-1543.
71. Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11: 40-45.
72. Saracco SA, Miller MJ, Kurepa J, Vierstra RD (2007) Genetic analysis of SUMOylation in Arabidopsis: conjugation of SUMO1 and SUMO2 to nuclear proteins is essential. Plant Physiol 145: 119-134.
73. Schenk PM, Kazan K, Manners JM, Anderson JP, Simpson RS, Wilson IW, Somerville SC, Maclean DJ (2003) Systemic gene expression in Arabidopsis during an incompatible interaction with Alternaria brassicicola. Plant Physiol 132: 999-1010.
74. Schultheiss H, Dechert C, Kogel KH, Hückelhoven R (2002) A small GTP-binding host protein is required for entry of powdery mildew fungus into epidermal cells of barley. Plant Physiol 128: 1447-1454.
75. Schultheiss H, Dechert C, Kogel KH, Hückelhoven R (2003) Functional analysis of barley RAC/ROP G-protein family members in susceptibility to the powdery mildew fungus. Plant J 36: 589-601.
76. Schulze-Lefert P, Panstruga R (2003) Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annu Rev Phytopathol 41: 641-667.
77. Schulze-Lefert P, Vogel J (2000) Closing the ranks to attack by powdery mildew. Trends Plant Sci 5: 343-348.
78. Schweizer P, Christoffel A, Dudler R (1999a) Transient expression of members of the germin-like gene family in epidermal cells of wheat confers disease resistance. Plant J 50: 541-552.
79. Schweizer P, Pokorny J, Abderhalden O, Dudler R (1999b) A transient assay system for the functional assessment of defense-related genes in wheat. Mol Plant Microbe Interact 12: 647-654.
80. Schweizer P, Pokorny J, Schulze-Lefert P, Dudler R (2000a) Double-stranded RNA interferes with gene function at the single-cell level in cereals. Plant J 24: 895-903.
81. Schweizer P, Kmecl A, Carpita N, Dudler R (2000b) A soluble carbohydrate elicitor from Blumeria graminis f. sp. tritici is recognized by a broad range of cereals. Physiol Mol Plant Pathol 56: 157-167.
82. Shinshi H, Neuhaus JM, Ryals J, Meins F Jr (1990) Structure of a tobacco endochitinase gene: evidence that different chitinase genes can arise by transposition of sequences encoding a cystein-rich domain. Plant Mol Biol 14: 357-368.
83. Smith M, Bhaskar V, Fernandez J, Courey AJ (2004) Drosophila Ulp1, a nuclear pore-associated SUMO protease, prevents accumulation of cytoplasmic SUMO conjugates. J Biol Chem 279: 43805-43814.
84. Spanu PD, Abbott JC, Amselem J et al (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330: 1543-1546.
85. Stein N, Perovic D, Kumlehn J, Pellio B, Stracke S, Streng S, Ordon F, Graner A (2005) The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant J 42: 912-922.
86. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4. 0. Mol Biol Evol 24: 1596-1599.
87. Tang DZ, Innes RW (2002) Overexpression of a kinase-deficient form of the EDR1 gene enhances powdery mildew resistance and ethylene-induced senescence in Arabidopsis. Plant J 32: 975-983.
88. Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou GZ, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringe. Plant Cell 15: 317-330.
89. Verger A, Perdomo J, Crossley M (2003) Modification with SUMO. A role in transcriptional regulation. EMBO Rep 4: 137-142.
90. Vogel J, Somerville S (2000) Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proc Natl Acad Sci USA 97: 1897-1902.
91. Vogel J, Raab TK, Schiff C, Somerville SC (2002) PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell 14: 2095-2106.
92. Vogel JP, Raab TK, Somerville CR, Somerville SC (2004) Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition. Plant J 40: 968-978.
93. Wang HY, Zhang ZS (1998) Occurrence degree and epidemic dynamics of powdery mildew on winter wheat varieties in Henan Province. Plant Protect 24: 6-9.
94. Wang XF, Zhang ZS, Liu HY, He WL (1996) Evaluation of resistance and slow-mildewing of some wheat varieties in Henan Province. Acta Agric Univ Henanensis 30: 160-163.
95. Winzeler M, Streckeisen P, Fried PM (1991) Virulence analysis of the wheat powdery mildew population in Switzerland between 1980 and 1989. In: Jørgensen JH (ed) Integrated control of cereal mildews: virulence patterns and their change. Risoe, Denmark, pp 15-21.
96. Xiong RY, Wu JX, Zhou YJ, Zhou XP (2009) Characterization and subcellular localization of an RNA silencing suppressor encoded by Rice stripe tenuivirus. Virology 387: 29-40.