Loss of Function in Mlo Orthologs Reduces Susceptibility of Pepper and Tomato to Powdery Mildew Disease Caused by Leveillula taurica

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Zheng, Zheng ^a   Nonomura, Teruo ^b   Appiano, Michela ^a,c   Pavan, Stefano ^c   Matsuda, Yoshinori ^b   Toyoda, Hideyoshi ^b   Wolters, Anne Marie A ^a   Visser, Richard G F ^a   Bai, Yuling ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b KINKI UNIVERSITY   (Japan)

^c UNIVERSITY OF BARI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA;

ARTICLE; CAMLO1 GENE; CAMLO2 GENE; CONTROLLED STUDY; DISEASE PREDISPOSITION; DISEASE RESISTANCE; DNA SEQUENCE; FUNGUS; GENE FREQUENCY; GENE FUNCTION; GENE ISOLATION; GENE LOSS; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; LEVEILLULA TAURICA; LOSS OF FUNCTION MUTATION; MLO GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OIDIUM NEOLYCOPERSICI; PEPPER; PHYLOGENY; PLANT GENE; POWDERY MILDEW; SINGLE NUCLEOTIDE POLYMORPHISM; SLMLO1 GENE; TOMATO; UPREGULATION;

AMINO ACID SEQUENCE; ASCOMYCOTA; BIOMASS; BREEDING; CAPSICUM; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PHENOTYPE; PHYLOGENY; PLANT DISEASES; PLANT PROTEINS; SEQUENCE ALIGNMENT; TRANSCRIPTION, GENETIC;

EID: 84880828734     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070723     Document Type: Article

References (52)

1. Braun U, (1987) A monograph of the Erysiphales (powdery mildews). Beih. Nova Hedwigia 89: 1-700.
2. Hewitt HG (1998) Fungicides in crop protection. CAB International, Wallingford, UK. 221.
3. Cerkauskas RF, Buonassisi A, (2003) First report of powdery mildew of greenhouse pepper caused by Leveillula taurica in British Columbia, Canada. Plant Dis 87: 1151-1151.
4. Chunwongse J, Bunn TB, Crossman C, Jiang J, Tanksley SD, (1994) Chromosomal localization and molecular-marker tagging of the powdery mildew resistance gene (Lv) in tomato. Theor Appl Genet 89: 76-79.
5. de Souza VL, Café-Filho AC, (2003) Resistance to Leveillula taurica in the genus Capsicum. Plant Pathol 52: 613-619.
6. Daubèze AM, Hennart JW, Palloix A, (1995) Resistance to Leveillula taurica in pepper (Capsicum annuum) is oligogenically controlled and stable in Mediterranean regions. Plant Breed 114: 327-332.
7. Shifriss C, Pilowsky M, Zacks J, (1992) Resistance to Leveillula taurica mildew (= Oidiopsis taurica) in Capsicum annuum. Phytoparasitica 20: 279-283.
8. Blat SF, da Costa CP, Vencovsky R, Sala FC, (2005) Reaction of sweet and hot pepper accesses to powdery mildew (Oidiopsis taurica). Hortic Bras 23: 72-75.
9. Lefebvre V, Daubèze AM, van der VoortJR, Peleman J, Bardin M, et al. (2003) QTLs for resistance to powdery mildew in pepper under natural and artificial infections. Theor Appl Genet 107: 661-666.
10. Fu X-L, Lu Y-G, Liu X-D, Li J-Q, (2009) Crossability barriers in the interspecific hybridization between Oryza sativa and O. meyeriana. J Integr Plant Biol 51: 21-28.
11. Xiao S, Charoenwattana P, Holcombe L, Turner JG, (2003) The Arabidopsis genes RPW8.1 and RPW8.2 confer induced resistance to powdery mildew diseases in tobacco. Mol Plant-Microbe Interact 16: 289-294.
12. Bent AF, (1996) Plant disease resistance genes: Function meets structure. The Plant Cell 8: 1757-1771.
13. Pavan S, Jacobsen E, Visser RGF, Bai Y, (2010) Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol Breeding 25: 1-12.
14. Eckardt NA, (2002) Plant disease susceptibility genes? The Plant Cell 14: 1983-1986.
15. Humphry M, Consonni C, Panstruga R, (2006) mlo-based powdery mildew immunity: silver bullet or simply non-host resistance? Mol Plant Pathol 7: 605-610.
16. Consonni C, Humphry ME, Hartmann HA, Livaja M, Durner J, et al. (2006) Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat Genet 38: 716-720.
17. Bai Y, Pavan S, Zheng Z, Zappel NF, Reinstädler A, et al. (2008) Naturally occurring broad-spectrum powdery mildew resistance in a central American tomato accession is caused by loss of Mlo function. Mol Plant-Microbe Interact 21: 30-39.
18. Humphry M, Reinstädler A, Ivanov S, Bisseling T, Panstruga R, (2011) Durable broad-spectrum powdery mildew resistance in pea er1 plants is conferred by natural loss-of-function mutations in PsMLO1. Mol Plant Pathol 12: 866-878.
19. Pavan S, Schiavulli A, Appiano M, Marcotrigiano AR, Cillo F, et al. (2011) Pea powdery mildew er1 resistance is associated to loss-of-function mutations at a MLO homologous locus. Theor Appl Genet 123: 1425-1431.
20. Pavan S, Zheng Z, Borisova M, van den Berg P, Lotti C, et al. (2008) Map- vs. homology-based cloning for the recessive gene ol-2 conferring resistance to tomato powdery mildew. Euphytica 162: 91-98.
21. Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, et al. (1997) The barley mlo gene: A novel control element of plant pathogen resistance. Cell 88: 695-705.
22. Devoto A, Piffanelli P, Nilsson I, Wallin E, Panstruga R, et al. (1999) Topology, subcellular localization, and sequence diversity of the Mlo family in plants. J Biol Chem 274: 34993-35004.
23. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB, (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11: 1187-1194.
24. Hückelhoven R, Trujillo M, Kogel K-H, (2000) Mutations in Ror1 and Ror2 genes cause modification of hydrogen peroxide accumulation in mlo-barley under attack from the powdery mildew fungus. Mol Plant Pathol 1: 287-292.
25. Hückelhoven R, Dechert C, Kogel K-H, (2001) Non-host resistance of barley is associated with a hydrogen peroxide burst at sites of attempted penetration by wheat powdery mildew fungus. Mol Plant Pathol 2: 199-205.
26. Feechan A, Jermakow AM, Torregrosa L, Panstruga R, Dry IB, (2008) Identification of grapevine MLO gene candidates involved in susceptibility to powdery mildew. Funct Plant Biol 35: 1255-1266.
27. Konishi S, Sasanuma T, Sasanuma T, (2010) Identification of novel Mlo family members in wheat and their genetic characterization. Genes Genet Syst 85: 167-175.
28. Devoto A, Hartmann HA, Piffanelli P, Elliott C, Simmons C, et al. (2003) Molecular phylogeny and evolution of the plant-specific seven-transmembrane MLO family. J Mol Evol 56: 77-88.
29. Liu Q, Zhu H, (2008) Molecular evolution of the MLO gene family in Oryza sativa and their functional divergence. Gene 409: 1-10.
30. Panstruga R, (2005) Discovery of novel conserved peptide domains by ortholog comparison within plant multi-protein families. Plant Mol Biol 59: 485-500.
31. Reinstädler A, Müller J, Czembor JH, Piffanelli P, Panstruga R, (2010) Novel induced mlo mutant alleles in combination with site-directed mutagenesis reveal functionally important domains in the heptahelical barley Mlo protein. BMC Plant Biol 10: 31.
32. Piffanelli P, Zhou F, Casais C, Orme J, Jarosch B, et al. (2002) The barley MLO modulator of defense and cell death is responsive to biotic and abiotic stress stimuli. Plant Physiol 129: 1076-1085.
33. Chen Z, Hartmann HA, Wu M-J, Friedman EJ, Chen J-G, et al. (2006) Expression analysis of the AtMLO gene family encoding plant-specific seven-transmembrane domain proteins. Plant Mol Biol 60: 583-597.
34. Elad Y, Messika Y, Brand M, Rav David D, Sztejnberg A, (2007) Effect of microclimate on Leveillula taurica powdery mildew of sweet pepper. Phytopathology 97: 813-824.
35. Kim DS, Hwang BK, (2012) The pepper MLO gene, CaMLO2, is involved in susceptibility cell death response and bacterial and oomycete proliferation. Plant J 72: 843-855.
36. Ashrafi H, Hill T, Stoffel K, Kozik A, Yao JQ, et al. (2012) De novo assembly of the pepper transcriptome (Capsicum annuum): a benchmark for in silico discovery of SNPs, SSRs and candidate genes. BMC Genomics 13: 571.
37. Jørgensen JH, (1992) Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica 63: 141-152.
38. The Tomato Genome Consortium, (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641.
39. Bai Y, Huang CC, van der Hulst R, Meijer-Dekens F, Bonnema G, et al. (2003) QTLs for tomato powdery mildew resistance (Oidium lycopersici) in Lycopersicon parviflorum G1.1601 co-localize with two qualitative powdery mildew resistance genes. Mol Plant-Microbe Interact 16: 169-176.
40. Zheng Z, Nonomura T, Bóka K, Matsuda Y, Visser RGF, et al. (2013) Detection and quantification of Leveillula taurica growth in pepper leaves. Phytopathology 103: 623-632.
41. Løvdal T, Lillo C, (2009) Reference gene selection for quantitative real-time PCR normalization in tomato subjected to nitrogen, cold, and light stress. Anal Biochem 387: 238-242.
42. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 -ΔΔCT method. Methods 25: 402-408.
43. Silvar C, Merino F, Díaz J, (2008) Differential activation of defense-related genes in susceptible and resistant pepper cultivars infected with Phytophthora capsici. J Plant Physiol 165: 1120-1124.
44. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucl Acids Res 36: W465-W469.
45. Wan H, Yuan W, Ruan M, Ye Q, Wang R, et al. (2011) Identification of reference genes for reverse transcription quantitative real-time PCR normalization in pepper (Capsicum annuum L.). Biochem Biophys Res Commun 416: 24-30.
46. Bin WS, Wei LK, Ping DW, Li Z, Wei G, et al. (2012) Evaluation of appropriate reference genes for gene expression studies in pepper by quantitative real-time PCR. Mol Breeding 30: 1393-1400.
47. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP, (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper - Excel-based tool using pair-wise correlations. Biotechnol Lett 26: 509-515.
48. Liu Y, Schiff M, (2002) Dinesh-Kumar (2002) Virus-induced gene silencing in tomato. Plant J 31: 777-786.
49. Nonomura T, Matsuda Y, Xu L, Kakutani K, Takikawa Y, et al. (2009) Collection of highly germinative pseudochain conidia of Oidium neolycopersici from conidiophores by electrostatic attraction. Mycol Res 113: 364-372.
50. Karimi M, Inze D, Depicker A, (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193-195.
51. Lazo GR, Stein PA, Ludwig RA, (1991) A DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Nature Biotech 9: 963-967.
52. McCormick S, Niedermeyer J, Fry J, Barnason A, Horsch R, et al. (1986) Leaf disc transformation of cultivated tomato (L. esculentum) using Agrobacterium tumefaciens. Plant Cell Rep 5: 81-84.