Theoretical and Applied Genetics

, Volume 131, Issue 1, pp 145–155 | Cite as

Linkage between the I-3 gene for resistance to Fusarium wilt race 3 and increased sensitivity to bacterial spot in tomato

  • Jian Li
  • Jessica Chitwood
  • Naama Menda
  • Lukas Mueller
  • Samuel F. Hutton
Original Article


Key message

The negative association between the I - 3 gene and increased sensitivity to bacterial spot is due to linkage drag (not pleiotropy) and may be remedied by reducing the introgression size.


Fusarium wilt is one of the most serious diseases of tomato (Solanum lycopersicum L.) throughout the world. There are three races of the pathogen (races 1, 2 and 3), and the deployment of three single, dominant resistance genes corresponding to each of these has been the primary means of controlling the disease. The I-3 gene was introgressed from S. pennellii and confers resistance to race 3. Although I-3 provides effective control, it is negatively associated with several horticultural traits, including increased sensitivity to bacterial spot disease (Xanthomonas spp.). To test the hypothesis that this association is due to linkage with unfavorable alleles rather than to pleiotropy, we used a map-based approach to develop a collection of recombinant inbred lines varying for portions of I-3 introgression. Progeny of recombinants were evaluated for bacterial spot severity in the field for three seasons, and disease severities were compared between I-3 introgression haplotypes for each recombinant. Results indicated that increased sensitivity to bacterial spot is not associated with the I-3 gene, but rather with an upstream region of the introgression. A survey of public and private inbred lines and hybrids indicates that the majority of modern I-3 germplasm contains a similarly sized introgression for which the negative association with bacterial spot likely persists. In light of this, it is expected that the development and utilization of a reduced I-3 introgression will significantly improve breeding efforts for resistance to Fusarium wilt race 3.



This research was supported in part by funding from the Florida Tomato Committee and the University of Florida Institute of Food and Agricultural Science (UF/IFAS). The authors thank D. A. Jones (The Australian National University) for providing the ‘M-82’ I-3 recombinant lines. We thank G.E. Vallad (UF/IFAS, Gulf Coast Research and Education Center) and members of his research team for providing Fol3 cultures and for conducting bacterial spot field inoculations. We also thank members of the UF/IFAS Tomato Breeding lab for their assistance with experiments.

Compliance with ethical standards


This research was supported in part by funding from the Florida Tomato Committee and the University of Florida Institute of Food and Agricultural Science (UF/IFAS).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

For this type of study formal consent is not required. This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

122_2017_2991_MOESM1_ESM.docx (3.5 mb)
Supplementary material 1 (DOCX 3586 kb)


  1. Alexander LJ (1959) Progress report of national screening committee for disease resistance in tomato for 1954–1957. Plant Dis Rptr 43:55–65Google Scholar
  2. Barillas AC, Mejia L, Sanchez-Perez A, Maxwell DP (2008) CAPS and SCAR markers for detection of I-3 gene introgression for resistance to Fusarium oxysporum f.sp. lycopersici race 3. Rep Tomato Genet Coop 58:11–17Google Scholar
  3. Bohn GW, Tucker CM (1939) Immunity to Fusarium wilt in the tomato. Science 89:603–604CrossRefPubMedGoogle Scholar
  4. Bolger A, Scossa F, Bolger ME, Lanz C, Maumus F, Tohge T, Quesneville H, Alseekh S, Sorensen I, Lichtenstein G, Fich EA, Conte M, Keller H, Schneeberger K, Schwacke R, Ofner I, Vrebalov J, Xu Y, Osorio S, Aflitos SA, Schijlen E, Jimenez-Gomez JM, Ryngajllo M, Kimura S, Kumar R, Koenig D, Headland LR, Maloof JN, Sinha N, van Ham RCHJ, Lankhorst RK, Mao L, Vogel A, Arsova B, Panstruga R, Fei Z, Rose JKC, Zamir D, Carrari F, Giovannoni JJ, Weigel D, Usadel B, Fernie AR (2014) The genome of the stress-tolerant wild tomato species Solanum pennellii. Nature Genetics 46:1034–1038CrossRefPubMedGoogle Scholar
  5. Bournival BL, Scott JW, Vallejos CE (1989) An isozyme marker for resistance to race 3 of Fusarium oxysporum f.sp. lycopersici in tomato. Theor Appl Genet 78:489–494CrossRefPubMedGoogle Scholar
  6. Brunner E, Puri ML (2001) Nonparametric methods in factorial designs. Stat Pap 42:1–52CrossRefGoogle Scholar
  7. Catanzariti AM, Lim GT, Jones DA (2015) The tomato I-3 gene: a novel gene for resistance to Fusarium wilt disease. New Phytol 207:106–118CrossRefPubMedGoogle Scholar
  8. Catanzariti AM, Do HTT, Bru P, de Sain M, Thatcher LF, Rep M, Jones DA (2017) The tomato I gene for Fusarium wilt resistance encodes an atypical leucine-rich repeat receptor-like protein whose function is nevertheless dependent on SOBIR1 and SERK3/BAK1. Plant J 89:1195–1209CrossRefPubMedGoogle Scholar
  9. Doyle JJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  10. Freeman JH, McAvoy EJ, Boyd NS, Dittmar PJ, Ozores-Hampton M, Smith HA, Vallad GE, Webb SE (2015) Vegetable production handbook of Florida 2015–2016. In: Freeman JH, Dittmar PJ, Vallad GE (eds) Tomato production. Vance Publishing Corporation, Lincolnshire, IL, pp 211–234Google Scholar
  11. Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rpt 13:207–209CrossRefGoogle Scholar
  12. Fulton T, van der Hoeven R, Eannetta N, Tanksley S (2002) Identification, analysis and utilization of a conserved ortholog set (COS) markers for comparative genomics in higher plants. Plant Cell 14:1457–1467CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gonzalez-Cendales Y, Catanzariti AM, Baker B, Mcgrath DJ, Jones DA (2016) Identification of I-7 expands the repertoire of genes for resistance to Fusarium wilt in tomato to three resistance gene classes. Mol Plant Pathol 17:448–463CrossRefPubMedGoogle Scholar
  14. Hemming MN, Basuki S, McGrath DJ, Carroll BJ, Jones DA (2004) Fine mapping of the tomato I-3 gene for Fusarium wilt resistance and elimination of a co-segregating resistance gene analogue as a candidate for I-3. Theor Appl Genet 109:409–418CrossRefPubMedGoogle Scholar
  15. Horsfall JG, Barratt RW (1945) An improved grading system for measuring plant diseases. Phytopathology 35:655Google Scholar
  16. Houterman PM, Cornelissen BJC, Martijn R (2008) Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathog 4(5):e1000061CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hutton SF, Scott JW, Jones JB (2010) Inheritance of resistance to bacterial spot race T4 from three tomato breeding lines with differing resistance backgrounds. J Amer Soc Hortic Sci 135:150–158Google Scholar
  18. Hutton SF, Scott JW, Vallad GE (2014) Association of Fusarium wilt race 3 resistance gene, I-3, on chromosome 7 with increased susceptibility to bacterial spot race T4 in tomato. J Amer Soc Hortic Sci 139:282–289Google Scholar
  19. Hutton SF, Ji Y, Scott JW (2015) Fla. 8923: a tomato breeding line with begomovirus resistance gene Ty-3 in a 70-kb Solanum chilense introgression. HorScience 50:1257–1259Google Scholar
  20. Jones JB, Bouzar H, Stall RE, Almira EC, Roberts PD, Bowen BW, Sudberry J, Strickler PM, Chun J (2000) Systematic analysis of xanthomonads (Xanthomonas spp.) associated with pepper and tomato lesions. Intl J Syst Evol Microbiol 50:1211–1219CrossRefGoogle Scholar
  21. Jones JB, Lacy GH, Bouzar H, Minsavage GV, Stall RE, Schaad NW (2005) Bacterial spot-worldwide distribution, importance and review. Acta Hort 695:27–33CrossRefGoogle Scholar
  22. Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291CrossRefPubMedGoogle Scholar
  23. Lim GTT, Wang GP, Hemming MN, Basuki S, McGrath DJ, Carroll BJ, Jones DA (2006) Mapping the I-3 gene for resistance to Fusarium wilt in tomato: application of an I-3 marker in tomato improvement and progress towards the cloning of I-3. Australas Plant Pathol 35:671–680CrossRefGoogle Scholar
  24. Lim GTT, Wang GP, Hemming MN, McGrath DJ, Jones DA (2008) High resolution genetic and physical mapping of the I-3 region of tomato chromosome 7 reveals almost continuous microsynteny with grape chromosome 12 but interspersed microsynteny with duplication on Arabidopsis chromosomes 1, 2 and 3. Theor Appl Genet 118:57–75CrossRefPubMedGoogle Scholar
  25. McGrath DJ, Gillespie D, Vawdrey L (1987) Inheritance of resistance to Fusarium oxysporum f.sp. lycopersici races 2 and 3 in Lycopersicon pennellii. Aust J Agr Res 38:729–733CrossRefGoogle Scholar
  26. Menda N, Strickler S, Edwards J, Bombarely A, Dunham D, Martin G, Mejia L, Hutton S, Havey M, Maxwell D, Mueller L (2014) Analysis of wild-species introgressions in tomato inbreds uncovers ancestral origins. BMC Plant Biol 14:287CrossRefPubMedPubMedCentralGoogle Scholar
  27. Pohronezny K, Volin RB (1983) The effect of bacterial spot on yield and quality of fresh-market tomatoes. HortScience 18:69–70Google Scholar
  28. Scott JW (1999) Tomato plants heterozygous for Fusarium wilt race 3 resistance develop larger fruit than homozygous resistant plants. Proc Fla State Hort Soc 112:305–307Google Scholar
  29. Scott JW (2004) Fla. 7946 tomato breeding line resistant to Fusarium oxysporum f.sp. lycopersici races 1, 2, and 3. HortScience 39:440–441Google Scholar
  30. Scott JW, Jones JB (1986) Sources of resistance to bacterial spot [Xanthomonas campestris pv. vesicatoria (Doidge) Dye] in tomato. HortScience 21:304–306Google Scholar
  31. Scott JW, Jones JP (1989) Monogenic resistance in tomato to Fusarium oxysporum f.sp. lycopersici race 3. Euphytica 40:49–53Google Scholar
  32. Scott JW, Jones JB (1995) Fla. 7547 and Fla. 7481 tomato breeding lines resistant to Fusarium oxysporum f.sp. lycopersici races 1, 2 and 3. HortScience 30:645–646Google Scholar
  33. Scott JW, Jones JP (2000) Fla. 7775 and Fla. 7781: tomato breeding lines resistant to Fusarium crown and root rot. HortScience 35:1183–1184Google Scholar
  34. Scott JW, Bartz JZ, Bryan HH, Everett PH, Gull DD, Howe TK, Stoffella PJ, Volin RB (1985) Horizon, a fresh market tomato with concentrated fruit set. Florida Agr Expt Sta Circ S-323Google Scholar
  35. Scott JW, Agrama HA, Jones JP (2004) RFLP-based analysis of recombination among resistance genes to fusarium wilt races 1, 2 and 3 in tomato. J Amer Soc Hort Sci 129:394–400Google Scholar
  36. Scott JW, Baldwin EA, Klee HJ, Brecht JK, Olson SM, Bartz JA, Sims CA (2008) Fla. 8153 hybrid tomato; Fla. 8059 and Fla. 7907 breeding lines. HortScience 43:2228–2230Google Scholar
  37. Shah DA, Madden LV (2004) Nonparametric analysis of ordinal data in designed factorial experiments. Phytopathology 94:33–43CrossRefPubMedGoogle Scholar
  38. Sim SC, Durstewitz G, Plieske J, Wieseke R, Ganal MW, Van Deynze A, Hamilton JP, Buell CR, Causse M, Wijeratne S, Francis DM (2012) Development of a large SNP genotyping array and generation of high-density genetic maps in tomato. PLoS One 7:e40563CrossRefPubMedPubMedCentralGoogle Scholar
  39. Simons G, Groenendijk J, Wijbrandi J, Reijans M, Groenen J, Diergaarde P, Van der Lee T, Bleeker M, Onstenk J, de Both M, Haring M, Mes J, Cornelissen B, Zabeau M, Vos P (1998) Dissection of the fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy. Plant Cell 10:1055–1068CrossRefPubMedPubMedCentralGoogle Scholar
  40. Stall RE, Walter JW (1965) Selection and inheritance of resistance in tomato to isolates of races 1 and 2 of the Fusarium wilt organism. Phytopathology 55:1213–1215Google Scholar
  41. Strickler SR, Bombarely A, Munkvold JD, York T, Menda N, Martin GB, Mueller LA (2015) Comparative genomics and phylogenetic discordance of cultivated tomato and close wild relatives. PeerJ. doi: 10.7717/peerj.793 PubMedPubMedCentralGoogle Scholar
  42. Thomas WB (1996) Methyl bromide: effective pest management tool and environmental threat. J Nematol 28:586–589PubMedPubMedCentralGoogle Scholar
  43. Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641CrossRefGoogle Scholar
  44. Vallad GE, Boyd N, Noling J (2014) A comparison of alternative fumigants to methyl bromide for Florida tomato. In: Proceedings from the 2014 annual international research conference on methyl bromide alternatives and emissions reductions, pp 6-1–6-4Google Scholar
  45. Wang GP, Lim GTT, Jones DA (2007) Development of PCR-based markers from the tomato glutamate oxaloacetate transaminase isozyme gene family as a means of revitalizing old isozyme markers and recruiting new ones. Mol Breeding 19:209–214CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Jian Li
    • 1
  • Jessica Chitwood
    • 1
  • Naama Menda
    • 2
  • Lukas Mueller
    • 2
  • Samuel F. Hutton
    • 1
  1. 1.Gulf Coast Research and Education Center, Institute of Food and Agricultural SciencesUniversity of FloridaWimaumaUSA
  2. 2.Boyce Thompson Institute for Plant ResearchIthacaUSA

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