Linkage between the I-3 gene for resistance to Fusarium wilt race 3 and increased sensitivity to bacterial spot in tomato
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.
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.
- Alexander LJ (1959) Progress report of national screening committee for disease resistance in tomato for 1954–1957. Plant Dis Rptr 43:55–65Google Scholar
- 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
- 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
- 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
- Doyle JJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
- 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
- Horsfall JG, Barratt RW (1945) An improved grading system for measuring plant diseases. Phytopathology 35:655Google Scholar
- 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
- 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
- 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
- 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
- Pohronezny K, Volin RB (1983) The effect of bacterial spot on yield and quality of fresh-market tomatoes. HortScience 18:69–70Google Scholar
- 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
- 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
- Scott JW, Jones JB (1986) Sources of resistance to bacterial spot [Xanthomonas campestris pv. vesicatoria (Doidge) Dye] in tomato. HortScience 21:304–306Google Scholar
- Scott JW, Jones JP (1989) Monogenic resistance in tomato to Fusarium oxysporum f.sp. lycopersici race 3. Euphytica 40:49–53Google Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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