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Identification of QTLs controlling resistance to Pseudomonas syringae pv. tomato race 1 strains from the wild tomato, Solanum habrochaites LA1777

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Screening of wild tomato accessions revealed a source of resistance to Pseudomonas syringe pv. tomato race 1 from Solanum habrochaites and facilitated mapping of QTLs controlling disease resistance.

Abstract

Pseudomonas syringae pv. tomato (Pst) causes bacterial speck of tomato, which is one of the most persistent bacterial diseases in tomato worldwide. Existing Pst populations have overcome genetic resistance mediated by the tomato genes Pto and Prf. The objective of this study was to identify sources of resistance to race 1 strains and map quantitative trait loci (QTLs) controlling resistance in the wild tomato Solanum habrochaites LA1777. Pst strains A9 and 407 are closely related to current field strains and genome sequencing revealed the lack of the avrPto effector as well as select mutations in the avrPtoB effector, which are recognized by Pto and Prf. Strains A9 and 407 were used to screen 278 tomato accessions, identifying five exhibiting resistance: S. peruvianum LA3799, S. peruvianum var. dentatum PI128655, S. chilense LA2765, S. habrochaites LA2869, and S. habrochaites LA1777. An existing set of 93 introgression lines developed from S. habrochaites LA1777 was screened for resistance to strain A9 in a replicated greenhouse trial. Four QTLs were identified using composite interval mapping and mapped to different chromosomes. bsRr1-1 was located on chromosome 1, bsRr1-2 on chromosome 2, and bsRr1-12a and bsRr1-12b on chromosome 12. The QTLs detected explained 10.5–12.5 % of the phenotypic variation. Promising lines were also subjected to bacterial growth curves to verify resistance and were analyzed for general horticultural attributes under greenhouse conditions. These findings will provide useful information for future high-resolution mapping of each QTL and integration into marker-assisted breeding programs.

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References

  • Almeida NF, Yan S, Lindeberg M, Studholme DJ, Schneider DJ, Condon B, Liu HJ, Viana CJ, Warren A, Evans C, Kemen E, MacLean D, Angot A, Martin GB, Jones JD, Collmer A, Setubal JC, Vinatzer BA (2009) A draft genome sequence of Pseudomonas syringae pv. tomato T1 reveals a type III effector repertoire significantly divergent from that of Pseudomonas syringae pv. tomato DC3000. Mol Plant Microbe Interact 22:52–62

    Article  CAS  PubMed  Google Scholar 

  • Arredondo CR, Davis RM (2000) First report of Pseudomonas syringae pv. tomato race 1 on tomato in California. Plant Dis 84:370–371

    Article  Google Scholar 

  • Astua-Monge G, Freitas-Astua J, Bacocina G, Roncoletta J, Carvalho SA, Machado MA (2005) Expression profiling of virulence and pathogenicity genes of Xanthomonas axonopodis pv. citri. J Bacteriol 187:1201–1205

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75

    Article  Google Scholar 

  • Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Mukhtar MS, Cherkis K, Roach J, Grant SR, Jones CD, Dangl JL (2011) Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathog 7:e1002132

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bart R, Cohn M, Kassen A, McCallum EJ, Shybut M, Petriello A, Krasileva K, Dahlbeck D, Medina C, Alicai T, Kumar L, Moreira LM, Neto JR, Verdier V, Santana MA, Kositcharoenkul N, Vanderschuren H, Gruissem W, Bernal A, Staskawicz BJ (2012) High-throughput genomic sequencing of cassava bacterial blight strains identifies conserved effectors to target for durable resistance. Proc Natl Acad Sci USA 109:E1972–E1979

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bernacchi D, Beck-Bunn T, Eshed Y, Lopez J, Petiard V, Uhlig J, Zamir D, Tanksley S (1998) Advanced backcross QTL analysis in tomato. I. Identification of QTLs for traits of agronomic importance from Lycopersicon hirsutum. Theor Appl Genet 97:381–397

    Article  CAS  Google Scholar 

  • Bogatsevska NS, Sotirova V, Stamova LD (1989) Race of Pseudomonas Syringae pv. tomato (Okabe) young Et-Al. Dokladi Na Bolgarskata Akademiya Na Naukite 42:129–130

    Google Scholar 

  • Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin AS, Kolonay JF, Madupu R, Daugherty S, Brinkac L, Beanan MJ, Haft DH, Nelson WC, Davidsen T, Zafar N, Zhou LW, Liu J, Yuan QP, Khouri H, Fedorova N, Tran B, Russell D, Berry K, Utterback T, Van Aken SE, Feldblyum TV, D’Ascenzo M, Deng WL, Ramos AR, Alfano JR, Cartinhour S, Chatterjee AK, Delaney TP, Lazarowitz SG, Martin GB, Schneider DJ, Tang XY, Bender CL, White O, Fraser CM, Collmer A (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci USA 100:10181–10186

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cai R, Lewis J, Yan S, Liu H, Clarke CR, Campanile F, Almeida NF, Studholme DJ, Lindeberg M, Schneider D, Zaccardelli M, Setubal JC, Morales-Lizcano NP, Bernal A, Coaker G, Baker C, Bender CL, Leman S, Vinatzer BA (2011) The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog 7:e1002130

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Canady MA, Meglic V, Chetelat RT (2005) A library of Solanum lycopersicoides introgression lines in cultivated tomato. Genome 48:685–697

    Article  CAS  PubMed  Google Scholar 

  • Castro AJ, Chen XM, Hayes PM, Johnston M (2003) Pyramiding quantitative trait locus (QTL) alleles determining resistance to barley stripe rust: effects on resistance at the seedling stage. Crop Sci 43:651–659

    Article  CAS  Google Scholar 

  • Darmon E, Leach DR (2014) Bacterial genome instability. Microbiol Mol Biol R 78:1–39

    Article  CAS  Google Scholar 

  • Delcher AL, Harmon D, Kasif S, White O, Salzberg SL (1999) Improved microbial gene identification with GLIMMER. Nucleic Acids Res 27:4636–4641

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Doganlar S, Frary A, Ku H-M, Tanksley SD (2002) Mapping quantitative trait loci in inbred backcross lines of Lycopersicon pimpinellifolium (LA1589). Genome 45:1189–1202

    Article  CAS  PubMed  Google Scholar 

  • Ercolano MR, Sanseverino W, Carli P, Ferriello F, Frusciante L (2012) Genetic and genomic approaches for R-gene mediated disease resistance in tomato: retrospects and prospects. Plant Cell Rep 31:973–985

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Eshed Y, Zamir D (1994) Introgressions from Lycopersicon pennellii can improve the soluble-solids yield of tomato hybrids. Theor Appl Genet 88:891–897

    Article  CAS  PubMed  Google Scholar 

  • Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141:1147–1162

    PubMed Central  CAS  PubMed  Google Scholar 

  • Eshed Y, Gera G, Zamir D (1996) A genome-wide search for wild-species alleles that increase horticultural yield of processing tomatoes. Theor Appl Genet 93:877–886

    Article  CAS  PubMed  Google Scholar 

  • Finkers R, van Heusden AW, Meijer-Dekens F, van Kan JA, Maris P, Lindhout P (2007) The construction of a Solanum habrochaites LYC4 introgression line population and the identification of QTLs for resistance to Botrytis cinerea. Theor Appl Genet 114:1071–1080

    Article  PubMed Central  PubMed  Google Scholar 

  • Foolad MR, Sharma A (2005) Molecular markers as selection tools in tomato breeding. Acta Hort (ISHS) 695:225–240

  • Francis DM, Kabelka E, Bell J, Franchino B, Clair D (2001) Resistance to bacterial canker in tomato (Lycopersicon hirsutum LA407) and its progeny derived from crosses to L. esculentum. Plant Dis 85:1171–1176

    Article  Google Scholar 

  • Fridman E, Carrari F, Liu YS, Fernie AR, Zamir D (2004) Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305:1786–1789

    Article  CAS  PubMed  Google Scholar 

  • Gabor BK, Frampton AJ, Bragaloni M, Tanksley SD (2010) Tomato plants that exhibit resistance to Botrytis cinerea. US7799976 B2, USA

  • Garcion C, Eveillard S, Renaudin J (2014) Characterisation of the tolerance to the beet leafhopper transmitted virescence agent phytoplasma in the PI128655 accession of Solanum peruvianum. Ann Appl Biol 165:236–248

    Article  Google Scholar 

  • Goode MJ, Sasser M (1980) Prevention—the key to controlling bacterial spot and bacterial speck of tomato. Phytopathology 64:831–834

    Google Scholar 

  • Grandillo S, Ku HM, Tanksley SD (1999) Identifying the loci responsible for natural variation in fruit size and shape in tomato. Theor Appl Genet 99:978–987

    Article  CAS  Google Scholar 

  • Hanson P, Sitathani K, Sadashiva A, Yang R-Y, Graham E, Ledesma D (2007) Performance of Solanum habrochaites LA1777 introgression line hybrids for marketable tomato fruit yield in Asia. Euphytica 158:167–178

    Article  Google Scholar 

  • Hassan S, Thomas PE (1988) Extreme resistance to tomato yellow top virus and potato leaf roll virus in Lycopersicon peruvianum and some of its tomato hybrids. Phytopathology 78:1164–1167

    Article  Google Scholar 

  • Hospital F (2005) Selection in backcross programmes. Phil Trans R Soc B 360:1503–1511. doi:10.1098/rstb.2005.1670

  • Ji Y, Chetelat RT (2007) GISH analysis of meiotic chromosome pairing in Solanum lycopersicoides introgression lines of cultivated tomato. Genome 50:825–833

    Article  CAS  PubMed  Google Scholar 

  • Keen NT, Tamaki S, Kobayashi D, Trollinger D (1998) Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70:191–197

    Article  Google Scholar 

  • Kim JF, Charkowski AO, Alfano JR, Collmer A, Beer SV (1998) Sequences related to transposable elements and bacteriophages flank avirulence genes of Pseudomonas syringae. Mol Plant Microbe Interact 11:1247–1252

    Article  CAS  Google Scholar 

  • Kunkeaw S, Tan S, Coaker G (2010) Molecular and evolutionary analyses of Pseudomonas syringae pv. tomato race 1. Mol Plant Microbe Interact 23:415–424

    Article  CAS  PubMed  Google Scholar 

  • Lawton MB, MacNeill BH (1986) Occurrence of race 1 of Pseudomonas syringae on field tomato in south western Ontario. Can J Plant Pathol 8:85–88

    Article  Google Scholar 

  • Li J, Liu L, Bai Y, Finkers R, Wang F, Du Y, Yang Y, Xie B, Visser RGF, Heusden A (2011) Identification and mapping of quantitative resistance to late blight (Phytophthora infestans) in Solanum habrochaites LA1777. Euphytica 179:427–438

    Article  Google Scholar 

  • Lin NC, Martin GB (2005) An avrPto/avrPtoB mutant of Pseudomonas syringae pv. tomato DC3000 does not elicit Pto-mediated resistance and is less virulent on tomato. Mol Plant Microbe Interact 18:43–51

    Article  CAS  PubMed  Google Scholar 

  • Lin NC, Abramovitch RB, Kim YJ, Martin GB (2006) Diverse AvrPtoB homologs from several Pseudomonas syringae pathovars elicit Pto-dependent resistance and have similar virulence activities. Appl Environ Microbiol 72:702–712

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu TY, Earle ED, Tanksley SD (1993) Map-based cloning of a protein-kinase gene conferring disease resistance in tomato. Science 262:1432–1436

    Article  CAS  PubMed  Google Scholar 

  • Mathieu S, Cin VD, Fei ZJ, Li H, Bliss P, Taylor MG, Klee HJ, Tieman DM (2009) Flavour compounds in tomato fruits: identification of loci and potential pathways affecting volatile composition. J Exp Bot 60:325–337

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Momotaz A, Scott JW, Schuster DJ (2005) Searching for silverleaf whitefly and begomovirus resistance genes from Lycopersicon hirsutum accession LA1777. Acta Hort (ISHS) 695:417–422

    Google Scholar 

  • Momotaz A, Scott J, Schuster D (2007a) Begomovirus resistance not found in Solanum habrochaites accession LA1777 recombinant inbred lines of tomato. HortScience 42:1015

    Google Scholar 

  • Momotaz A, Scott JW, Schuster DJ (2007b) Solanum habrochaites accession LA1777 recombinant inbred lines are not resistant to tomato yellow leaf curl virus or tomato mottle virus. HortScience 42:1149–1152

    CAS  Google Scholar 

  • Monforte AJ, Tanksley SD (2000) Development of a set of near isogenic and backcross recombinant inbred lines containing most of the Lycopersicon hirsutum genome in a L. esculentum genetic background: a tool for gene mapping and gene discovery. Genome 43:803–813

    Article  CAS  PubMed  Google Scholar 

  • Monforte AJ, Friedman E, Zamir D, Tanksley SD (2001) Comparison of a set of allelic QTL-NILs for chromosome 4 of tomato: deductions about natural variation and implications for germplasm utilization. Theor Appl Genet 102:572–590

    Article  CAS  Google Scholar 

  • Muigai SG, Schuster DJ, Snyder JC, Scott JW, Bassett MJ, McAuslane HJ (2002) Mechanisms of resistance in Lycopersicon germplasm to the whitefly Bemisia argentifolii. Phytoparasitica 30:347–360

    Article  Google Scholar 

  • Pedley KF, Martin GB (2003) Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Annu Rev Phytopathol 41:215–243

    Article  CAS  PubMed  Google Scholar 

  • Pilowsky MaZ D (1982) Screening wild tomatoes for resistance to bacterial speck pathogen (Pseudomonas tomato). Plant Dis 66:46–47

    Article  Google Scholar 

  • Pitblado RE, Kerr EA (1979) A source of resistance to bacterial speck Pseudomonas tomato. Tomato Genet Coop Rep 29:30

    Google Scholar 

  • Pitblado RE, Kerr EA (1980) Resistance to bacterial speck (Pseudomonas tomato) in tomato. Acta Hort (ISHS) 100:379–382

    Google Scholar 

  • Robertson L, Labate J (2007) Genetic resources of tomato (Lycopersicon esculentum var. esculentum) and wild relatives. In: Razdan M, Mattoo A (eds) Genetic Improvement of Solanaceous Crops, Enfield, USA, pp 25–75

  • Rousseaux MC, Jones CM, Adams D, Chetelat R, Bennett A, Powell A (2005) QTL analysis of fruit antioxidants in tomato using Lycopersicon pennellii introgression lines. Theor Appl Genet 111:1396–1408

    Article  CAS  PubMed  Google Scholar 

  • Salmeron JM, Barker SJ, Carland FM, Mehta AY, Staskawicz BJ (1994) Tomato mutants altered in bacterial disease resistance provide evidence for a new locus controlling pathogen recognition. Plant Cell 6:511–520

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • SAS Institute (2011) SAS/STAT 9.3 user’s guide. SAS Institute Inc, Cary, NC

  • Schauer N, Semel Y, Roessner U, Gur A, Balbo I, Carrari F, Pleban T, Perez-Melis A, Bruedigam C, Kopka J, Willmitzer L, Zamir D, Fernie AR (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol 24:447–454

    Article  CAS  PubMed  Google Scholar 

  • Scott J, Gardner R (2007) Breeding for resistance to fungal pathogens. Genetic Improvement of Solanaceous Crops, Enfield, NH, pp 421–453

    Google Scholar 

  • Smart CD, Tanksley SD, Mayton H, Fry WE (2007) Resistance to Phytophthora infestans in Lycopersicon pennellii. Plant Dis 91:1045–1049

    Article  Google Scholar 

  • Stockinger EJ, Walling LL (1994) Pto3 and Pto4: novel genes from Lycopersicon hirsutum var. glabratum that confer resistance to Pseudomonas syringae pv. tomato. Theor Appl Genet 89:879–884

    CAS  PubMed  Google Scholar 

  • Tanksley SD, Grandillo S, Fulton TM, Zamir D, Eshed Y, Petiard V, Lopez J, BeckBunn T (1996) Advanced backcross QTL analysis in a cross between an elite processing line of tomato and its wild relative L. pimpinellifolium. Theor Appl Genet 92:213–224

    Article  CAS  PubMed  Google Scholar 

  • Thomas PE, Boll RK (1978) Tolerance to curly top virus in tomato. Phytopathology 12:181

    Google Scholar 

  • Vidavsky F, Czosnek H (1998) Tomato breeding lines resistant and tolerant to tomato yellow leaf curl virus issued from Lycopersicon hirsutum. Phytopathology 88:910–914

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Basten CJ, Zeng ZB (2012) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm

  • Wulff BB, Horvath DM, Ward ER (2011) Improving immunity in crops: new tactics in an old game. Curr Opin Plant Biol 14:468–476

    Article  CAS  PubMed  Google Scholar 

  • Xing W, Zou Y, Liu Q, Liu J, Luo X, Huang Q, Chen S, Zhu L, Bi R, Hao Q, Wu J-W, Zhou J-M, Chai J (2007) The structural basis for activation of plant immunity by bacterial effector protein AvrPto. Nature 449:243–247

  • Yunis H, Bashan Y, Okon Y, Henis Y (1980) Weather dependence, yield losses, and control of bacterial speck of tomato caused by Peudomonas tomato. Plant Dis 64:937–939

    Article  Google Scholar 

  • Zamir D (2001) Improving plant breeding with exotic genetic libraries. Nat Rev Genet 2:983–989

    Article  CAS  PubMed  Google Scholar 

  • Zamir D, Eshed Y (1998) Case history in germplasm introgression: Tomato genetics and breeding using nearly isogenic introgression lines derive d from wild species. In: Press CRC (ed) Paterson AH. New, York, pp 207–217

    Google Scholar 

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Acknowledgments

This work was supported by the California Tomato Research Institute grants awarded to GC and a USDA-ARS grant (under the parent project “Conservation and Utilization of Germplasm of Selected Vegetable Crops”) awarded to GM. We thank the Tomato Genetics Resource Center and the USDA-ARS Plant Genetic Resources Unit, Geneva, New York for providing tomato seed. We thank members of the Coaker lab for critically reading the manuscript.

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The authors declare that they have no conflict of interest.

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The authors declare that the study complies with the current laws of the country in which they were performed.

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Correspondence to Gitta Coaker.

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Communicated by Glenn James Bryan.

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122_2015_2463_MOESM1_ESM.tif

Fig. S1. Bacterial growth curve analyses of introgression lines exhibiting reduced symptom progression after inoculation with P. syringae pv. tomato strain A9 that did not contain detected QTLs. Plants included the wild tomato S. habrochaites accession LA1777 and the recurrent parent S. lycopersicum E6203. Four-week-old tomato plants were dip inoculated with strain A9 at a concentration of 1 × 108 CFU/ml. a Disease symptoms were photographed 4 days post-inoculation. b Bacterial growth curves were conducted 4 days post-inoculation. Results are shown as the mean (n = 3), ± standard deviation. Statistical differences were detected by Fisher’s least significant difference (α = 0.05). (TIFF 1065 kb)

122_2015_2463_MOESM2_ESM.tiff

Fig. S2. Phenotypic variation in fruit from selected tomato genotypes exhibiting resistance to P. syringae pv. tomato strain A9. (TIFF 564 kb)

Table S1. Wild tomato accessions screened for resistance to P. syringae pv. tomato race 1. (PDF 77 kb)

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Thapa, S.P., Miyao, E.M., Michael Davis, R. et al. Identification of QTLs controlling resistance to Pseudomonas syringae pv. tomato race 1 strains from the wild tomato, Solanum habrochaites LA1777. Theor Appl Genet 128, 681–692 (2015). https://doi.org/10.1007/s00122-015-2463-7

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