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Marker-assisted Selection to Combine Alleles for Four Disease Resistance Genes of Tomato Collocated on Chromosome 11

Authors:
Caleb J. Orchard Department of Horticulture and Crop Science, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691, USA

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Jonathan Kressin Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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Suchada Chompookam Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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Jutharat Chuapong Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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Namfon Onmanee Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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Karina Van Leeuwen Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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Darush Struss Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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Conrado Balatero Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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David M. Francis Department of Horticulture and Crop Science, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691, USA

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Abstract

Bacterial, fungal, and viral diseases of tomato (Solanum lycopersicum) are responsible for widespread yield losses, especially in humid growing environments. Chromosome 11 of tomato contains genes that modulate resistance to several prominent tomato pathogens, including bacterial spot caused by Xanthomonas spp., gray leaf spot caused by Stemphylium spp., Fusarium wilt caused by race 2 of Fusarium oxysporum f. sp. lycopersici, and tomato yellow leaf curl virus (TYLCV) caused by begomoviruses. Major resistance loci are quantitative trait locus 11 (QTL-11) and Xv3/Rx4 for bacterial spot, Sm for gray leaf spot, I2 for Fusarium wilt, and Ty-2 for TYLCV. Marker-assisted selection was used to select for rare recombination events that combined these resistance loci into a linked cassette that can be inherited together in future crosses. A pedigree breeding strategy was used with marker-assisted selection and used to identify a novel coupling of Xv3/Rx4 and Ty-2. Recombination between the two genes was estimated as 0.056 cM, demonstrating that effective combinations of resistance can be established using publicly available germplasm. Progeny from the recombinant plants were screened using inoculated seedling trials to confirm resistance. The recombinants identified maintained resistance levels similar to the resistant controls. Trial results suggest that the trait markers on chromosome 11 are tightly linked to the respective resistance loci and are effective for selecting plants with resistance to the target diseases.

Plant diseases cause an estimated 20% to 40% loss in annual global crop production (FAO 2019). Mixed infections of bacterial, fungal, and viral diseases are common in tomatoes (Solanum lycopersicum) grown in humid subtropical and tropical environments, causing severe defoliation and fruit damage in areas as dispersed as the North American Great Lakes to South East Asia (Jones et al. 2014; Ma et al. 2011; Prasad et al. 2020; Saha and Das 2012).

Mixed infections of pathogens require breeders to select for combinations of resistances. The clustering of resistance loci has been well-documented in plants from Zea mays to Arabidopsis thaliana (McMullen and Simcox 1995; Michelmore and Meyers 1998; Wisser et al. 2006). Among breeding lines, resistance loci for separate diseases may be contributed by different parents in the pedigree but located on the same chromosome and, therefore, linked in repulsion. Selection for coupling phase recombination events that combine resistance genes or quantitative trait loci (QTL) on the same chromosome can create cassettes of resistance loci that will be inherited together in future crosses (Robbins et al. 2010; Yang and Francis 2005). After a linked cassette of resistance genes has been created, it may be deployed into a breeding strategy to recombine with cassettes or genes located on other chromosomes.

Marker-assisted selection (MAS) is routinely used to track and select for combinations of genes and QTL. Sequence-based markers linked to separate resistance loci identify not only recombination but also the subset of recombinants likely to contain both resistances. Markers allow for the visualization and selection of rare recombination events that would be difficult to identify using trait data. MAS has been effectively used in tomato for decades as a technique to introduce novel resistance from a wild tomato relative to an adapted variety and to pyramid resistance genes (Bolkan et al. 1987; Rick 1974). MAS was used to combine the resistance genes Rx-3 and Pto on chromosome 5, conferring resistance to Xanthomonas euvesicatoria race T1 and Pseudomonas syringae pv. tomato, respectively (Yang and Francis 2005). A similar strategy was used to combine spotted wilt virus (Sw5) resistance and Phytophthora infestans (Ph3) resistance in the coupling phase (Robbins et al. 2010).

Chromosome 11 of tomato contains resistance genes to several important diseases that routinely occur in humid and tropical environments. One such disease is bacterial spot caused by Xanthomonas spp. Multiple bacterial spot resistance loci originating from wild tomato species and breeding lines have been mapped to chromosome 11. The resistance locus Xv3/Rx4, derived from H7981, PI 128216, and other Solanum pimpinellifolium accessions (Robbins et al. 2009; Scott et al. 1996; Scott et al. 1997; Wang et al. 2011) provides resistance to X. perforans race T3 (Minsavage et al. 1996; Pei et al. 2012; Scott et al. 1996). A QTL conferring nonspecific resistance to bacterial spot was identified on chromosome 11 (Hutton et al. 2010; Scott et al. 1997; Sim et al. 2015; Yang et al. 2005). QTL-11 appears to exist as an allelic series with distinct resistance alleles (and/or QTL) identified in H7998, PI 114490, and S. pimpinellifolium accession LA2533 (Bernal et al. 2020; Liabeuf et al. 2018; Sim et al. 2015). The combination of QTL-11 and Xv3/Rx4 has been incorporated in modern processing breeding lines (Bernal et al. 2020). Resistance to the fungal disease gray leaf spot caused by Stemphylium spp. also maps to chromosome 11 (Behare et al. 1991). The incompletely dominant gene, Sm, was originally discovered in Solanum pimpinellifolium accession PI 79532 (Andrus et al. 1942) and has been widely used by breeders to control gray leaf spot for more than 60 years. Ty-2 is located ∼1.2 Mbp from Xv3/Rx4 on chromosome 11, and it is one of several genes conferring resistance to tomato yellow leaf curl virus (TYLCV) caused by begomoviruses (Yamaguchi et al. 2018; Yang et al. 2014). Ty-2 and Xv3/Rx4 are linked in repulsion, and recombination between the two genes is expected to be rare. Nearby Ty-2 lies the I2 gene that confers resistance to Fusarium wilt caused by race 2 of Fusarium oxysporum f. sp. lycopersici (Laterrot 1976). I2 has been introgressed into cultivated tomato from S. pimpinellifolium (Stall and Walter 1965). Breeding lines with the combination of Ty-2 and I2 genes in the coupling phase were developed as part of a multiple disease resistance breeding program (Hanson et al. 2016).

The objective of this research was to create novel combinations of resistance genes and QTL for bacterial, fungal, and viral diseases on chromosome 11 for humid and tropical tomato markets. Chromosome 11 was chosen as the target for recombination because resistance to bacterial spot (QTL-11 and Xv3/Rx4), gray leaf spot (Sm), geminivirus (Ty-2), and Fusarium wilt (I2) all map to this chromosome. We specifically aimed to create a novel coupling phase recombination between Xv3/Rx4 and Ty-2. Because both genes are used as part of multigene resistance packages against diseases with complex genetic control, creating a coupling phase combination allows them to be transferred together. This project combined processing germplasm developed for the Midwestern United States with a line bred for tropical production to create recombinant lines containing resistance to four major pathogens.

Materials and Methods

Plant material.

Two parent lines were used as donors of the target genes and QTL for resistance on chromosome 11. OH08-7663 is a processing tomato line developed at The Ohio State University that contains Xv3/Rx4 inherited from PI 128216 (Robbins et al. 2009; Wang et al. 2011). OH08-7663 is derived from a complex population (Sim et al. 2015) and also contains QTL-11 inherited from accession H7998 via Fla. 7600 (Hutton et al. 2010; Scott et al. 2003). TH-35506 is a fresh market tomato line contributed from East-West Seed Company and contains Sm for resistance to gray leaf spot, Ty-2 for resistance to TYLCV, and I2 for resistance to Fusarium wilt. TH-35506 was chosen for its heat adaptability, as well as its desirable plant habit and fruit quality characteristics for tropical fresh market tomato production. Genotyping the two parent lines revealed that OH08-7663 also carries the Sm gene, whereas TH-35506 contains QTL-11. TH-35506 and OH08-7663 were crossed and the hybrid was self-pollinated to create an F2 population for recombinant selection.

Seedlings from the F2 generation were grown in 72-cell plastic trays in a net house at East-West Seed Company facilities in Chiang Mai, Thailand. Selected F2 seedlings were transplanted into 20- × 33-cm plastic bags containing a 3:2 coconut coir:coconut piece growing media. Plants were grown to harvest and seeds were collected from ripe fruit. Selections were advanced in subsequent generations in net house trials under similar growing conditions. Multiple single-plant selections were made from each F3 family to produce F4 lines for validation trials. Both F4 and F5 lines were used in validation trials. Target genes and QTL were monitored using trait-linked molecular markers throughout generation advancement and before transplanting.

DNA isolation and marker analysis.

Leaf tissue was collected from individual F2 seedlings into 96-well plates. Genomic DNA was extracted from leaf tissue using a cetyltrimethylammonium bromide extraction method (Doyle and Doyle 1987) with volumes scaled for 96-well format (Sim et al. 2015). Genotyping was performed by allele-specific polymerase chain reaction using Kompetitive allele-specific polymerase chain reaction according to manufacturer protocols (LGC Genomics, Berlin, Germany). A thermo cycler (Soellex® high-throughput polymerase chain reaction thermal cycler; Douglas Scientific, Alexandria, MN, USA) was used to process Kompetitive allele-specific polymerase chain reaction assays in 384 cell array tape with the following cycling conditions: denaturation at 95 °C for 15 min; nine cycles of 95 °C for 20 s; touchdown starting at 65 °C for 60 s (decreasing 0.8 °C per cycle); and followed by 30 to 40 cycles of amplification (95 °C for 20 s; 57 °C for 60 s). Endpoint fluorescence data were visualized with a light scanner (Araya machine; Douglas Scientific) and analyzed using KlusterCaller software (LGC Genomics, Berlin, Germany). DNA isolation and genotyping were performed at East-West Seed Company facilities in Chiang Mai, Thailand.

Information regarding the mapping and position of linked markers for QTL-11, Xv3/Rx4, Sm, Ty-2, and I2 has been published previously (Bernal et al. 2020; Ji and Scott 2009; Pei et al. 2012; Popoola et al. 2014; Yang et al. 2014). Single-nucleotide polymorphism (SNP) markers for QTL-11, Xv3/Rx4, Sm, Ty-2, and I2 developed in-house at East-West Seed were used to genotype individuals. A single SNP marker per target gene was used to genotype individuals for Xv3/Rx4, Sm, Ty-2, and I2, whereas three SNP markers spanning the target region were used for QTL-11. A collection of SNP markers developed at East-West Seed and as part of the Solanaceae Coordinated Agricultural Project were used to genotype selected individuals along the entire chromosome 11 (Hamilton et al. 2012; Sim et al. 2012).

F2 recombinant analysis.

A total of 5079 F2 plants were genotyped for the recombinant analysis. After removing plants with missing data for one or more of the markers, 4748 plants remained for the Xv3/Rx4 and Ty-2 analysis, and 4744 plants remained for the Ty-2 and I-2 analysis. Recombination frequencies were calculated using the est.rf function in the R/qtl package in R (R Core Team 2021), which implements a version of the expectation-maximization algorithm (Broman et al. 2003).

Greenhouse and field experiments.

Recombinant selections underwent separate greenhouse evaluations for Fusarium wilt (F. oxysporum f. sp. lycopersici race 2), gray leaf spot (S. lycopersici), and bacterial spot (X. perforans race T3). Greenhouse trials were conducted using a randomized complete block design consisting of two blocks containing 12 plants per block in the Fusarium wilt trial and 15 plants per block in the gray leaf spot and bacterial spot trials. A separate bacterial spot hypersensitive response (HR) test used two blocks with three plants per block and four leaves per plant. All trials were conducted at East-West Seed facilities in Chiang Mai, Thailand.

Gray leaf spot.

Inoculum containing spores of a single spore-derived strain of S. lycopersici from Thailand and used for routine screening were applied to 3-week-old seedlings using a spray inoculation method (Yang et al. 2017). Individual plant ratings were taken at 14 d after inoculation. Plants were rated using a scale of 0 to 4, with 0 corresponding to symptomless plants, and 1, 2, 3, and 4 given to plants displaying 1% to 25%, 26% to 50%, 51% to 75%, and 76% to 100% infection levels, respectively. Disease severity scores were calculated for each entry according to the number of plants in each rating category, and the scores were used to evaluate resistance. Accessions ‘Bonny Best’ (CO-02188; PI 153746) and ‘Moneymaker’ (CO-00564; LA2706) were used as susceptible controls, whereas ‘Walter’ (CO-01813; LA3465) and ‘Campbell 28’ (CO-01803; LA3317) were used as resistant controls (Behare et al. 1991). Accessions with CO and TH codes are from the collection of East-West Seed. PI numbers are from the USDA National Plant Germplasm System (GRIN Global). LA numbers are from the C. M. Rick Tomato Genetics Resource Center (University of California, Davis).

Bacterial spot spray inoculation.

Spray inoculation of 3-week-old seedlings was performed in the greenhouse (Du et al. 2014). The inoculum contained a local X. perforans race T3 strain from Thailand used for routine screening. Plants were evaluated individually at 14 d after inoculation using a scale from 0 to 4 (0 = no symptoms; 1 = 1% to 25% infection; 2 = 26% to 50%; 3 = 51% to 75%; and 4 = 76% to 100%). Disease severity scores were calculated for each entry according to the number of plants in each rating category, and the scores were used to evaluate resistance. ‘Bonny Best’ and ‘Peto 94’ were used as susceptible controls. Accessions H7998 (LA3856) and H7981 (LA4441) acted as intermediate and resistant controls, respectively (Robbins et al. 2009).

Bacterial spot HR.

In the greenhouse, 5-week-old seedlings were inoculated with a local X. perforans race T3 strain from Thailand used for routine screening using methods described previously (Baimei et al. 2015; Burlakoti et al. 2018). A 1-mL syringe without the needle was used for infiltration through the back of a fully expanded leaflet on four true leaves per plant. Plants were kept in a humid environment and HR was recorded 5 d after inoculation. Accessions ‘Bonny Best’ and ‘Walter’ were used as susceptible controls, whereas H7981 was the resistant control (Robbins et al. 2009).

Fusarium wilt.

The 2-week-old seedlings were inoculated with a local strain of F. oxysporum f. sp. lycopersici using a root-dip method in which plant roots were dipped into inoculum for 15 s before transplanting (Li et al. 2022; Scott et al. 2004). Individual plant ratings were taken at 21 d using a rating scale of 0 to 4 (0 = healthy, no symptoms; 4 = severe symptoms or dead). Disease severity scores were calculated for each entry according to the number of plants in each rating category, and the scores were used to evaluate resistance. Accessions ‘UC82-L’ (TH-39719) and ‘MH-1’ (TH-39720) were used as susceptible and resistant controls, respectively.

Statistical analysis.

The disease severity data for the inoculated seedling trials for gray leaf spot, bacterial spot, and Fusarium wilt were not normally distributed; therefore, a statistical analysis to determine if differences existed between accessions was conducted using a nonparametric Kruskal-Wallis test. Multiple comparisons were performed using Dunn’s test as implemented in the FSA package (Ogle et al. 2022). All analyses were performed using R statistical software (R Core Team 2021).

Results and Discussion

This work used two parents with specific coupling phase resistance gene combinations on chromosome 11 (Table 1). Parent line OH08-7663 is the result of crossing Ohio lines developed from introgression breeding programs for bacterial spot and bacterial speck with lines from the Florida breeding program as described previously (Fig. 1) (Sim et al. 2015). OH08-7763 was developed as a processing tomato line and contains QTL-11 and Xv3/Rx-4 in the coupling phase, conditioning resistance to bacterial spot. Parent line TH-35506 is a fresh-market tomato line contributed by East-West Seed that contains the coupling phase combination of Ty-2 and I2. The complementary coupling phase gene combinations present in both parents enabled the direct selection of desired recombinants containing all four resistance alleles.

Fig. 1.
Fig. 1.

Pedigree of recombinant tomato selections that contain a cassette of resistances on chromosome 11 to four major pathogens. The recombinant selections were derived from a cross between a processing tomato line (OH08-7663) and a fresh-market line (TH-35506) bred for tropical production.

Citation: HortScience 58, 5; 10.21273/HORTSCI16982-22

Table 1.

Molecular marker profiles of tomato parental lines OH08-7663 and TH-35506, F1 hybrid, and recombinant selections containing coupling phase recombination events on chromosome 11.

Table 1.

Coupling phase recombinant selection.

We used markers to monitor specific recombination events on chromosome 11 with the goal of identifying recombinants that combine resistance genes and QTL from different parents. A total of 5079 F2 plants were genotyped for recombinant analysis using SNP markers for Xv3/Rx4, Ty-2, and I2, conferring resistance to bacterial spot race T3, TYLCV, and Fusarium wilt race 2, respectively. Two plants were identified with homozygous coupling phase recombination events for the resistant alleles of Xv3/Rx4, Ty-2, and I2. Although Ty-2 and I2 were already linked in the coupling phase in the parent line TH-35506, the recombination between Xv3/Rx4 and Ty-2 is novel and addresses two important diseases in humid tropical environments. Four plants had the opposing homozygous double recombination event with the susceptible alleles of Xv3/Rx4, Ty-2, and I2. An additional 289 plants were fixed for the resistant allele of one of the target markers and heterozygous for the others. We observed segregation distortion from the expected 1:2:1 ratio at P = 0.05 (χ2 = 263.64 for Xv3/Rx4; χ2 = 319.32 for Ty-2). Considering the source of Xv3/Rx4 (S. pimpinellifolium) and Ty-2 (S. habrochaites), segregation distortion is not unexpected. Skewed segregation was also reported previously in the Ty-2 introgression region from S. habrochaites (Yang et al. 2014).

In the two selected F2 plants, recombination occurred in a region on chromosome 11 between 47.1 and 53.1 Mbp (Fig. 2). We estimated recombination between the Xv3/Rx4 and Ty-2 markers as 0.056 cM for this cross. The distance between Xv3/Rx4 and Ty-2 linked markers was estimated to be ∼10 cM according to the EXPIM 2012 map (Fig. 3) (Sim et al. 2012). Recombination is population-specific, which may explain the difference between the two estimates. Recombination between Ty-2 and I2 was estimated to be 0.00032 cM. The low rate of recombination between Ty-2 and I2 makes it difficult to estimate the relative order of these resistance loci in our cross. Because resistance genes are often members of multigene families, as is the case with the I2 gene, the order of loci may change depending on the number of homologs segregating in a specific cross (Simons et al. 1998). The close linkage between Xv3/Rx4, Ty2, and I2 suggests a low probability for the separation of the desirable resistance alleles in subsequent crosses.

Fig. 2.
Fig. 2.

Haplotypes along tomato chromosome 11 for parental controls OH08-7663 and TH-35506, F1 hybrid, and F2 recombinant selections containing coupling-phase recombination events. Single-nucleotide polymorphism (SNP) marker genotypes are labeled as A for the OH08-7663 allele, H for heterozygous, B for the TH-35506 allele, and for missing. Shading indicates the OH08-7663 allele. Monomorphic SNPs have been removed except when they provide pertinent information for resistance or chromosome scale.

Citation: HortScience 58, 5; 10.21273/HORTSCI16982-22

Fig. 3.
Fig. 3.

Physical and genetic positions of single-nucleotide polymorphism (SNP) markers on chromosome 11 of tomato. Labels indicate marker positions of disease resistance genes and quantitative trait loci (QTL) monitored for recombination with physical and genetic positions listed in parentheses.

Citation: HortScience 58, 5; 10.21273/HORTSCI16982-22

The two recombinant F2 plants, parent lines, and the F1 hybrid were genotyped with additional markers to observe haplotypes across chromosome 11 (Fig. 2). In addition to Xv3/Rx4, Ty-2, and I2, the double recombinants also carried the resistant alleles of QTL-11 and Sm. Both parent lines contained the resistant alleles of QTL-11 and Sm; therefore, these loci were not segregating in the F2 population. All F2 plants were genotyped with three SNPs to monitor potential recombination within QTL-11; however, no recombination was found, consistent with the location of these loci near the centromere region of chromosome 11 (Sim et al. 2012). The combination of QTL-11, Sm, Rx4-Xv3, Ty-2, and I2 on chromosome 11 creates a novel cassette containing resistance to four diseases. Lines containing the cassette can be transferred to elite germplasm for further evaluation using MAS or whole-genome-based selection approaches (Bernal et al. 2020; Orchard et al. 2021). However, because the cassette delineated by markers spans ∼33 cM, polymorphisms should be used to monitor progeny to ensure that the cassette remains intact during the breeding process.

Performance of selected recombinants for disease resistance.

After selection with markers, we confirmed resistance in the recombinants using inoculated seedling trials for gray leaf spot, bacterial spot, and Fusarium wilt (Table 2). Seed was saved from individual F3 plants, and F3:4 or F3:5 plants were used for disease trials.

Table 2.

Disease resistance of parental lines OH08-7663 and TH-35506, F1 hybrid, two recombinant selections, and controls determined by molecular markers and/or seedling inoculations.

Table 2.

In the gray leaf spot trial, lines carrying Sm were resistant during evaluation at 14 d after inoculation with S. lycopersici. The recombinant selections behaved as expected, with severity scores (1.3–1.5) similar to those of the resistant controls ‘Walter’ (Sm) and ‘Campbell 28’ (Sm), and significantly different from those of the susceptible controls ‘Bonny Best’ and ‘Money Maker’ (P ≤ 0.05). Because both parent lines carry Sm, which has been effective against gray leaf spot since it was deployed in cultivated tomato more than 60 years ago, it was not unexpected that the resistance transferred to the recombinant selections (Andrus et al. 1942).

To confirm resistance to bacterial spot caused by X. perforans race T3, we evaluated the recombinant selections based on an HR and in a spray-inoculated seedling trial. Xv3/Rx4 elicited an HR response in the recombinants and also contributed to a reduction in infection levels. In the HR trial, susceptible controls ‘Peto94’, ‘Bonny Best’, and parent line TH-35506 displayed water-soaked lesions at 5 d after infestation with a northern Thailand strain of X. perforans race T3. The recombinant selections, resistant control H7981 (Xv3), and parent line OH08-7663 showed an HR within 3 d. The F1 hybrid had a mixed reaction with some plants showing an HR, whereas others were susceptible. In the spray-inoculated trial, the recombinant plants behaved similarly, with severity scores (1.6) comparable to those of the resistant control H7981. Achieving broad-spectrum resistance to bacterial spot is challenging because of the complex genetic control of resistance and rapidly shifting pathogen populations (Bernal et al. 2022; Rotondo et al. 2022). Combinations of bacterial spot resistance genes and QTL (Bernal et al. 2020; Sim et al. 2015), such as QTL-11 and Xv3/Rx4 present in parent line OH08-7663, aim to combat rapid shifts in pathogenicity or virulence. Bacterial spot symptom severity was reduced in the recombinants with QTL-11 and Xv3/Rx4 as compared with the susceptible controls, as expected, but disease was not prevented.

Because of the severity of TYLCV pressure in Thailand, plants with a single TYLCV resistance gene appear susceptible, preventing the evaluation of Ty-2 individually. Ty-2-mediated resistance is ineffective against bipartite begomoviruses and some strains of TYLCV, requiring the gene to be combined with other TYLCV resistance genes (Barbieri et al. 2010; Ji et al. 2007; Mejía et al. 2004; Ohnishi et al. 2016; Yang et al. 2014). Therefore, a marker was used to confirm the presence of Ty-2 in the recombinant selections. Both recombinant selections contain the Ty-2 marker, but Recombinant Selection #1B also contains the Ty-1 marker. In field trials in Thailand, the two gene combination of Ty-1 and Ty-2 was enough to prevent severe disease symptoms in Recombinant Selection #1B, whereas Recombinant Selection #2C plants were susceptible (data not shown). The presence of two dominant TYLCV resistance genes in Recombinant Selection #1B provides a foundation to add more TYLCV resistance genes via pyramiding or in hybrid combinations (Ji et al. 2009).

To confirm the effect of the I2 gene, which imparts resistance to Fusarium wilt caused by race 2 of F. oxysporum f. sp. lycopersici, recombinant plants were tested in an inoculated seedling trial. The resistant control ‘MH-1’ (I2) and susceptible control ‘UC82-L’ showed expected reactions to F. oxysporum f. sp. lycopersici at 21 d after inoculation. The two recombinant selections and parent line TH-35506 were resistant (scores = 0). I2 and Ty-2 are located ∼0.4 Mbp from one another on chromosome 11, but the two genes are frequently linked in repulsion in breeding germplasm (Yang et al. 2014). The marker genotypes and phenotypes described here confirm the coupling phase linkage of these loci in select germplasm.

Conclusion

Pyramiding resistances to multiple diseases offers a strategy to combat mixed infections in humid growing environments. When resistance loci are linked in repulsion, targeted experiments to create coupling phase linkage events can be pursued in tandem with the routine breeding program. We demonstrate that publicly available germplasm such as OH08-7663 can be used to create and select favorable coupling phase recombination events that pyramid resistance loci on the same chromosome. A similar approach can be implemented on other chromosomes to combine beneficial resistance genes.

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  • Ji, Y, Scott, JW & Schuster, DJ 2009 Toward fine mapping of the tomato yellow leaf curl virus resistance gene Ty-2 on chromosome 11 of tomato HortScience. 44 3 614 618 https://doi.org/10.21273/HORTSCI.44.3.614

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  • Jones, J, Zitter, T, Momol, T & Miller, S 2014 Compendium of tomato diseases and pests 2nd ed American Phytopathological Society St. Paul, Minnesota, USA https://doi.org/10.1094/9780890544341

    • Search Google Scholar
    • Export Citation
  • Laterrot, H 1976 Mapping of I2 in tomato, controlling the resistance to pathotype 2 of Fusariumoxysporum f. Lycopersici Ann Amelior Plant. 26 3 485 491

    • Search Google Scholar
    • Export Citation
  • Li, J, Chitwood-Brown, J, Kaur, G, Labate, JA, Vallad, GE, Lee, TG & Hutton, SF 2022 Novel sources of resistance to Fusarium oxysporum f. sp. lycopersici race 3 among Solanum pennellii accessions J Am Soc Hortic Sci. 147 1 35 44 https://doi.org/10.21273/JASHS05080-21

    • Search Google Scholar
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  • Liabeuf, D, Sim, S-C & Francis, DM 2018 Comparison of marker-based genomic estimated breeding values and phenotypic evaluation for selection of bacterial spot resistance in tomato Phytopathology. 108 3 392 401 https://doi.org/10.1094/PHYTO-12-16-0431-R

    • Search Google Scholar
    • Export Citation
  • Ma, X, Lewis Ivey, ML & Miller, SA 2011 First report of Xanthomonas gardneri causing bacterial spot of tomato in Ohio and Michigan Plant Dis. 95 12 1584 https://doi.org/10.1094/PDIS-05-11-0448

    • Search Google Scholar
    • Export Citation
  • McMullen, M & Simcox, K 1995 Genomic organization of disease and insect resistance genes in maize Mol Plant Microbe Interact. 8 811 815

  • Mejía, L, Teni, RE, Vidavski, F, Czosnek, H, Lapidot, M, Nakhla, MK & Maxwell, DP 2004 Evaluation of tomato germplasm and selection of breeding lines for resistance to begomoviruses in Guatemala Acta Hortic. 695 251 256 https://doi.org/10.17660/ActaHortic.2005.695.27

    • Search Google Scholar
    • Export Citation
  • Michelmore, RW & Meyers, BC 1998 Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process Genome Res. 8 11 1113 1130 https://doi.org/10.1101/gr.8.11.1113

    • Search Google Scholar
    • Export Citation
  • Minsavage, G, Jones, J & Stall, R 1996 Cloning and sequencing of an avirulence gene (avrRxv3) isolated from Xanthomonas campestris pv. vesicatoria tomato race 3 Phytopathology. 86 S15

    • Search Google Scholar
    • Export Citation
  • Ogle, DH, Doll, JC, Wheeler, P & Dinno, A 2022 FSA: fisheries stock analysis R package version 0.9.3. https://github.com/fishR-Core-Team/FSA

  • Ohnishi, J, Yamaguchi, H & Saito, A 2016 Analysis of the mild strain of tomato yellow leaf curl virus, which overcomes Ty-2 gene–mediated resistance in tomato line H24 Arch Virol. 161 8 2207 2217 https://doi.org/10.1007/s00705-016-2898-4

    • Search Google Scholar
    • Export Citation
  • Orchard, CJ, Cooperstone, JL, Gas-Pascual, E, Andrade, MC, Abud, G, Schwartz, SJ & Francis, DM 2021 Identification and assessment of alleles in the promoter of the Cyc-b gene that modulate levels of β-carotene in ripe tomato fruit Plant Genome. 14 1 e20085 https://doi.org/10.1002/tpg2.20085

    • Search Google Scholar
    • Export Citation
  • Pei, C, Wang, H, Zhang, J, Wang, Y, Francis, DM & Yang, W 2012 Fine mapping and analysis of a candidate gene in tomato accession PI128216 conferring hypersensitive resistance to bacterial spot race T3 Theor Appl Genet. 124 3 533 542 https://doi.org/10.1007/s00122-011-1726-1

    • Search Google Scholar
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  • Popoola, A, Ercolano, M, Ferriello, F, Kaledzi, P, Kwoseh, C, Ganiyu, S, Ojo, D, Adegbite, D & Falana, Y 2014 Caps markers TAO1 and TG105 in the identification of I2 resistant gene in Nigerian accessions of tomato, Solanum lycopersicum L Niger J Biotechnol. 28 43 51

    • Search Google Scholar
    • Export Citation
  • Prasad, A, Sharma, N, Hari-Gowthem, G, Muthamilarasan, M & Prasad, M 2020 Tomato yellow leaf curl virus: Impact, challenges, and management Trends Plant Sci. 25 9 897 911 https://doi.org/10.1016/j.tplants.2020.03.015

    • Search Google Scholar
    • Export Citation
  • R Core Team 2021 A language and environment for statistical computing R foundation for statistical computing. Vienna, Austria R Foundation for Statistical Computing

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    • Export Citation
  • Rick, C 1974 Association of an allozyme with nematode resistance Tomato Genet Coop Rep. 24 25

  • Robbins, MD, Darrigues, A, Sim, S-C, Masud, MA & Francis, DM 2009 Characterization of hypersensitive resistance to bacterial spot race T3 (Xanthomonas perforans) from tomato accession PI 128216 Phytopathology. 99 9 1037 1044 https://doi.org/10.1094/PHYTO-99-9-1037

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    • Export Citation
  • Robbins, MD, Masud, MA, Panthee, DR, Gardner, RG, Francis, DM & Stevens, MR 2010 Marker-assisted selection for coupling phase resistance to tomato spotted wilt virus and Phytophthora infestans (late blight) in tomato HortScience. 45 10 1424 1428 https://doi.org/10.21273/HORTSCI.45.10.1424

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    • Export Citation
  • Rotondo, F, Bernal, E, Ma, X, Ivey, MLL, Sahin, F, Francis, DM & Miller, SA 2022 Shifts in Xanthomonas spp. causing bacterial spot in processing tomato in the Midwest of the United States Can J Plant Pathol. 44 5 652 667 https://doi.org/10.1080/07060661.2022.2047788

    • Search Google Scholar
    • Export Citation
  • Saha, P & Das, S 2012 Assessment of yield loss due to early blight (Alternaria solani) in tomato Indian J Plant Prot. 40 195 198

  • Scott, J, Miller, S, Stall, R, Jones, J, Somodi, G, Barbosa, V, Francis, D & Sahin, F 1997 Resistance to race T2 of the bacterial spot pathogen in tomato HortScience. 32 4 724 727 https://doi.org/10.21273/HORTSCI.32.4.724

    • Search Google Scholar
    • Export Citation
  • Scott, J, Stall, R, Jones, J & Somodi, G 1996 A single gene controls the hypersensitive response of Hawaii 7981 to race 3 (T3) of the bacterial spot pathogen Tomato Genet Coop Rep. 46 23

    • Search Google Scholar
    • Export Citation
  • 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 Am Soc Hortic Sci. 129 3 394 400 https://doi.org/10.21273/JASHS.129.3.0394

    • Search Google Scholar
    • Export Citation
  • Scott, JW, Francis, DM, Miller, SA, Somodi, GC & Jones, JB 2003 Tomato bacterial spot resistance derived from PI 114490; inheritance of resistance to race T2 and relationship across three pathogen races J Am Soc Hortic Sci. 128 5 698 703 https://doi.org/10.21273/JASHS.128.5.0698

    • Search Google Scholar
    • Export Citation
  • Sim, S-C, Durstewitz, G, Plieske, J, Wieseke, R, Ganal, MW, Van Deynze, A, Hamilton, JP, Buell, CR, Causse, M & Wijeratne, S 2012 Development of a large SNP genotyping array and generation of high-density genetic maps in tomato PLoS One. 7 7 e40563 https://doi.org/10.1371/journal.pone.0040563

    • Search Google Scholar
    • Export Citation
  • Sim, S-C, Robbins, MD, Wijeratne, S, Wang, H, Yang, W & Francis, DM 2015 Association analysis for bacterial spot resistance in a directionally selected complex breeding population of tomato Phytopathology. 105 11 1437 1445 https://doi.org/10.1094/PHYTO-02-15-0051-R

    • Search Google Scholar
    • Export Citation
  • Simons, G, Groenendijk, J, Wijbrandi, J, Reijans, M, Groenen, J, Diergaarde, P, Van der Lee, T, Bleeker, M, Onstenk, J & de Both, M 1998 Dissection of the Fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy Plant Cell. 10 6 1055 1068 https://doi.org/10.1105/tpc.10.6.1055

    • Search Google Scholar
    • Export Citation
  • Stall, R & Walter, J 1965 Selection and inheritance of resistance in tomato to isolates of races 1 and 2 of Fusarium wilt organism Phytopathology. 55 11 1213 1215

    • Search Google Scholar
    • Export Citation
  • Wang, H, Hutton, SF, Robbins, MD, Sim, S-C, Scott, JW, Yang, W, Jones, JB & Francis, DM 2011 Molecular mapping of hypersensitive resistance from tomato ‘Hawaii 7981’ to Xanthomonas perforans race T3 Phytopathology. 101 10 1217 1223 https://doi.org/10.1094/PHYTO-12-10-0345

    • Search Google Scholar
    • Export Citation
  • Wisser, RJ, Balint-Kurti, PJ & Nelson, RJ 2006 The genetic architecture of disease resistance in maize: A synthesis of published studies Phytopathology. 96 2 120 129 https://doi.org/10.1094/PHYTO-96-0120

    • Search Google Scholar
    • Export Citation
  • Yamaguchi, H, Ohnishi, J, Saito, A, Ohyama, A, Nunome, T, Miyatake, K & Fukuoka, H 2018 An NB-LRR gene, TYNBS1, is responsible for resistance mediated by the Ty-2 Begomovirus resistance locus of tomato Theor Appl Genet. 131 6 1345 1362 https://doi.org/10.1007/s00122-018-3082-x

    • Search Google Scholar
    • Export Citation
  • Yang, H, Zhao, T, Jiang, J, Wang, S, Wang, A, Li, J & Xu, X 2017 Mapping and screening of the tomato Stemphylium lycopersici resistance gene, Sm, based on bulked segregant analysis in combination with genome resequencing BMC Plant Biol. 17 1 266 https://doi.org/10.1186/s12870-017-1215-z

    • Search Google Scholar
    • Export Citation
  • Yang, W & Francis, DM 2005 Marker-assisted selection for combining resistance to bacterial spot and bacterial speck in tomato J Am Soc Hortic Sci. 130 5 716 721 https://doi.org/10.21273/JASHS.130.5.716

    • Search Google Scholar
    • Export Citation
  • Yang, W, Sacks, EJ, Lewis Ivey, ML, Miller, SA & Francis, DM 2005 Resistance in Lycopersicon esculentum intraspecific crosses to race T1 strains of Xanthomonas campestris pv. Vesicatoria causing bacterial spot of tomato Phytopathology. 95 5 519 527 https://doi.org/10.1094/PHYTO-95-0519

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  • Yang, X, Caro, M, Hutton, SF, Scott, JW, Guo, Y, Wang, X, Rashid, MH, Szinay, D, de Jong, H & Visser, RG 2014 Fine mapping of the tomato yellow leaf curl virus resistance gene Ty-2 on chromosome 11 of tomato Mol Breed. 34 2 749 760 https://doi.org/10.1007/s11032-014-0072-9

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  • Fig. 1.

    Pedigree of recombinant tomato selections that contain a cassette of resistances on chromosome 11 to four major pathogens. The recombinant selections were derived from a cross between a processing tomato line (OH08-7663) and a fresh-market line (TH-35506) bred for tropical production.

  • Fig. 2.

    Haplotypes along tomato chromosome 11 for parental controls OH08-7663 and TH-35506, F1 hybrid, and F2 recombinant selections containing coupling-phase recombination events. Single-nucleotide polymorphism (SNP) marker genotypes are labeled as A for the OH08-7663 allele, H for heterozygous, B for the TH-35506 allele, and for missing. Shading indicates the OH08-7663 allele. Monomorphic SNPs have been removed except when they provide pertinent information for resistance or chromosome scale.

  • Fig. 3.

    Physical and genetic positions of single-nucleotide polymorphism (SNP) markers on chromosome 11 of tomato. Labels indicate marker positions of disease resistance genes and quantitative trait loci (QTL) monitored for recombination with physical and genetic positions listed in parentheses.

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  • Baimei, Z, Haipeng, C, Junjie, D & Wencai, Y 2015 Allelic tests and sequence analysis of three genes for resistance to Xanthomonas perforans race T3 in tomato Hortic Plant J. 1 1 41 47 https://doi.org/10.16420/j.issn.2095-9885.2015-0001

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  • Bernal, E, Rotondo, F, Roman-Reyna, V, Klass, T, Timilsina, S, Minsavage, GV, Iruegas-Bocardo, F, Goss, EM, Jones, JB, Jacobs, JM, Miller, SA & Francis, DM 2022 Migration drives the replacement of Xanthomonas perforans races in the absence of widely deployed resistance Front Microbiol. 13 826386 https://doi.org/10.3389/fmicb.2022.826386

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  • Du, H, Li, W, Wang, Y & Yang, W 2014 Identification of genes differentially expressed between resistant and susceptible tomato lines during time-course interactions with Xanthomonas perforans race T3 PLoS One. 9 3 e93476 https://doi.org/10.1371/journal.pone.0093476

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  • Hamilton, JP, Sim, SC, Stoffel, K, Van Deynze, A, Buell, CR & Francis, DM 2012 Single nucleotide polymorphism discovery in cultivated tomato via sequencing by synthesis Plant Genome. 5 1 https://doi.org/10.3835/plantgenome2011.12.0033

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  • Hanson, P, Lu, S-F, Wang, J-F, Chen, W, Kenyon, L, Tan, C-W, Tee, KL, Wang, Y-Y, Hsu, Y-C & Schafleitner, R 2016 Conventional and molecular marker-assisted selection and pyramiding of genes for multiple disease resistance in tomato Scientia Hortic. 201 346 354 https://doi.org/10.1016/j.scienta.2016.02.020

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  • Hutton, SF, Scott, JW, Yang, W, Sim, S-C, Francis, DM & Jones, JB 2010 Identification of QTL associated with resistance to bacterial spot race T4 in tomato Theor Appl Genet. 121 7 1275 1287 https://doi.org/10.1007/s00122-010-1387-5

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  • Ji, Y, Schuster, DJ & Scott, JW 2007 Ty-3, a begomovirus resistance locus near the tomato yellow leaf curl virus resistance locus Ty-1 on chromosome 6 of tomato Mol Breed. 20 3 271 284 https://doi.org/10.1007/s11032-007-9089-7

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  • Ji, Y & Scott, J 2009 A caps marker linked to the tomato gray leaf spot (Stemphylium sp.) resistance gene Sm Tomato Genet Coop Rep. 59 29 31

  • Ji, Y, Scott, JW & Schuster, DJ 2009 Toward fine mapping of the tomato yellow leaf curl virus resistance gene Ty-2 on chromosome 11 of tomato HortScience. 44 3 614 618 https://doi.org/10.21273/HORTSCI.44.3.614

    • Search Google Scholar
    • Export Citation
  • Jones, J, Zitter, T, Momol, T & Miller, S 2014 Compendium of tomato diseases and pests 2nd ed American Phytopathological Society St. Paul, Minnesota, USA https://doi.org/10.1094/9780890544341

    • Search Google Scholar
    • Export Citation
  • Laterrot, H 1976 Mapping of I2 in tomato, controlling the resistance to pathotype 2 of Fusariumoxysporum f. Lycopersici Ann Amelior Plant. 26 3 485 491

    • Search Google Scholar
    • Export Citation
  • Li, J, Chitwood-Brown, J, Kaur, G, Labate, JA, Vallad, GE, Lee, TG & Hutton, SF 2022 Novel sources of resistance to Fusarium oxysporum f. sp. lycopersici race 3 among Solanum pennellii accessions J Am Soc Hortic Sci. 147 1 35 44 https://doi.org/10.21273/JASHS05080-21

    • Search Google Scholar
    • Export Citation
  • Liabeuf, D, Sim, S-C & Francis, DM 2018 Comparison of marker-based genomic estimated breeding values and phenotypic evaluation for selection of bacterial spot resistance in tomato Phytopathology. 108 3 392 401 https://doi.org/10.1094/PHYTO-12-16-0431-R

    • Search Google Scholar
    • Export Citation
  • Ma, X, Lewis Ivey, ML & Miller, SA 2011 First report of Xanthomonas gardneri causing bacterial spot of tomato in Ohio and Michigan Plant Dis. 95 12 1584 https://doi.org/10.1094/PDIS-05-11-0448

    • Search Google Scholar
    • Export Citation
  • McMullen, M & Simcox, K 1995 Genomic organization of disease and insect resistance genes in maize Mol Plant Microbe Interact. 8 811 815

  • Mejía, L, Teni, RE, Vidavski, F, Czosnek, H, Lapidot, M, Nakhla, MK & Maxwell, DP 2004 Evaluation of tomato germplasm and selection of breeding lines for resistance to begomoviruses in Guatemala Acta Hortic. 695 251 256 https://doi.org/10.17660/ActaHortic.2005.695.27

    • Search Google Scholar
    • Export Citation
  • Michelmore, RW & Meyers, BC 1998 Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process Genome Res. 8 11 1113 1130 https://doi.org/10.1101/gr.8.11.1113

    • Search Google Scholar
    • Export Citation
  • Minsavage, G, Jones, J & Stall, R 1996 Cloning and sequencing of an avirulence gene (avrRxv3) isolated from Xanthomonas campestris pv. vesicatoria tomato race 3 Phytopathology. 86 S15

    • Search Google Scholar
    • Export Citation
  • Ogle, DH, Doll, JC, Wheeler, P & Dinno, A 2022 FSA: fisheries stock analysis R package version 0.9.3. https://github.com/fishR-Core-Team/FSA

  • Ohnishi, J, Yamaguchi, H & Saito, A 2016 Analysis of the mild strain of tomato yellow leaf curl virus, which overcomes Ty-2 gene–mediated resistance in tomato line H24 Arch Virol. 161 8 2207 2217 https://doi.org/10.1007/s00705-016-2898-4

    • Search Google Scholar
    • Export Citation
  • Orchard, CJ, Cooperstone, JL, Gas-Pascual, E, Andrade, MC, Abud, G, Schwartz, SJ & Francis, DM 2021 Identification and assessment of alleles in the promoter of the Cyc-b gene that modulate levels of β-carotene in ripe tomato fruit Plant Genome. 14 1 e20085 https://doi.org/10.1002/tpg2.20085

    • Search Google Scholar
    • Export Citation
  • Pei, C, Wang, H, Zhang, J, Wang, Y, Francis, DM & Yang, W 2012 Fine mapping and analysis of a candidate gene in tomato accession PI128216 conferring hypersensitive resistance to bacterial spot race T3 Theor Appl Genet. 124 3 533 542 https://doi.org/10.1007/s00122-011-1726-1

    • Search Google Scholar
    • Export Citation
  • Popoola, A, Ercolano, M, Ferriello, F, Kaledzi, P, Kwoseh, C, Ganiyu, S, Ojo, D, Adegbite, D & Falana, Y 2014 Caps markers TAO1 and TG105 in the identification of I2 resistant gene in Nigerian accessions of tomato, Solanum lycopersicum L Niger J Biotechnol. 28 43 51

    • Search Google Scholar
    • Export Citation
  • Prasad, A, Sharma, N, Hari-Gowthem, G, Muthamilarasan, M & Prasad, M 2020 Tomato yellow leaf curl virus: Impact, challenges, and management Trends Plant Sci. 25 9 897 911 https://doi.org/10.1016/j.tplants.2020.03.015

    • Search Google Scholar
    • Export Citation
  • R Core Team 2021 A language and environment for statistical computing R foundation for statistical computing. Vienna, Austria R Foundation for Statistical Computing

    • Search Google Scholar
    • Export Citation
  • Rick, C 1974 Association of an allozyme with nematode resistance Tomato Genet Coop Rep. 24 25

  • Robbins, MD, Darrigues, A, Sim, S-C, Masud, MA & Francis, DM 2009 Characterization of hypersensitive resistance to bacterial spot race T3 (Xanthomonas perforans) from tomato accession PI 128216 Phytopathology. 99 9 1037 1044 https://doi.org/10.1094/PHYTO-99-9-1037

    • Search Google Scholar
    • Export Citation
  • Robbins, MD, Masud, MA, Panthee, DR, Gardner, RG, Francis, DM & Stevens, MR 2010 Marker-assisted selection for coupling phase resistance to tomato spotted wilt virus and Phytophthora infestans (late blight) in tomato HortScience. 45 10 1424 1428 https://doi.org/10.21273/HORTSCI.45.10.1424

    • Search Google Scholar
    • Export Citation
  • Rotondo, F, Bernal, E, Ma, X, Ivey, MLL, Sahin, F, Francis, DM & Miller, SA 2022 Shifts in Xanthomonas spp. causing bacterial spot in processing tomato in the Midwest of the United States Can J Plant Pathol. 44 5 652 667 https://doi.org/10.1080/07060661.2022.2047788

    • Search Google Scholar
    • Export Citation
  • Saha, P & Das, S 2012 Assessment of yield loss due to early blight (Alternaria solani) in tomato Indian J Plant Prot. 40 195 198

  • Scott, J, Miller, S, Stall, R, Jones, J, Somodi, G, Barbosa, V, Francis, D & Sahin, F 1997 Resistance to race T2 of the bacterial spot pathogen in tomato HortScience. 32 4 724 727 https://doi.org/10.21273/HORTSCI.32.4.724

    • Search Google Scholar
    • Export Citation
  • Scott, J, Stall, R, Jones, J & Somodi, G 1996 A single gene controls the hypersensitive response of Hawaii 7981 to race 3 (T3) of the bacterial spot pathogen Tomato Genet Coop Rep. 46 23

    • Search Google Scholar
    • Export Citation
  • 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 Am Soc Hortic Sci. 129 3 394 400 https://doi.org/10.21273/JASHS.129.3.0394

    • Search Google Scholar
    • Export Citation
  • Scott, JW, Francis, DM, Miller, SA, Somodi, GC & Jones, JB 2003 Tomato bacterial spot resistance derived from PI 114490; inheritance of resistance to race T2 and relationship across three pathogen races J Am Soc Hortic Sci. 128 5 698 703 https://doi.org/10.21273/JASHS.128.5.0698

    • Search Google Scholar
    • Export Citation
  • Sim, S-C, Durstewitz, G, Plieske, J, Wieseke, R, Ganal, MW, Van Deynze, A, Hamilton, JP, Buell, CR, Causse, M & Wijeratne, S 2012 Development of a large SNP genotyping array and generation of high-density genetic maps in tomato PLoS One. 7 7 e40563 https://doi.org/10.1371/journal.pone.0040563

    • Search Google Scholar
    • Export Citation
  • Sim, S-C, Robbins, MD, Wijeratne, S, Wang, H, Yang, W & Francis, DM 2015 Association analysis for bacterial spot resistance in a directionally selected complex breeding population of tomato Phytopathology. 105 11 1437 1445 https://doi.org/10.1094/PHYTO-02-15-0051-R

    • Search Google Scholar
    • Export Citation
  • Simons, G, Groenendijk, J, Wijbrandi, J, Reijans, M, Groenen, J, Diergaarde, P, Van der Lee, T, Bleeker, M, Onstenk, J & de Both, M 1998 Dissection of the Fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy Plant Cell. 10 6 1055 1068 https://doi.org/10.1105/tpc.10.6.1055

    • Search Google Scholar
    • Export Citation
  • Stall, R & Walter, J 1965 Selection and inheritance of resistance in tomato to isolates of races 1 and 2 of Fusarium wilt organism Phytopathology. 55 11 1213 1215

    • Search Google Scholar
    • Export Citation
  • Wang, H, Hutton, SF, Robbins, MD, Sim, S-C, Scott, JW, Yang, W, Jones, JB & Francis, DM 2011 Molecular mapping of hypersensitive resistance from tomato ‘Hawaii 7981’ to Xanthomonas perforans race T3 Phytopathology. 101 10 1217 1223 https://doi.org/10.1094/PHYTO-12-10-0345

    • Search Google Scholar
    • Export Citation
  • Wisser, RJ, Balint-Kurti, PJ & Nelson, RJ 2006 The genetic architecture of disease resistance in maize: A synthesis of published studies Phytopathology. 96 2 120 129 https://doi.org/10.1094/PHYTO-96-0120

    • Search Google Scholar
    • Export Citation
  • Yamaguchi, H, Ohnishi, J, Saito, A, Ohyama, A, Nunome, T, Miyatake, K & Fukuoka, H 2018 An NB-LRR gene, TYNBS1, is responsible for resistance mediated by the Ty-2 Begomovirus resistance locus of tomato Theor Appl Genet. 131 6 1345 1362 https://doi.org/10.1007/s00122-018-3082-x

    • Search Google Scholar
    • Export Citation
  • Yang, H, Zhao, T, Jiang, J, Wang, S, Wang, A, Li, J & Xu, X 2017 Mapping and screening of the tomato Stemphylium lycopersici resistance gene, Sm, based on bulked segregant analysis in combination with genome resequencing BMC Plant Biol. 17 1 266 https://doi.org/10.1186/s12870-017-1215-z

    • Search Google Scholar
    • Export Citation
  • Yang, W & Francis, DM 2005 Marker-assisted selection for combining resistance to bacterial spot and bacterial speck in tomato J Am Soc Hortic Sci. 130 5 716 721 https://doi.org/10.21273/JASHS.130.5.716

    • Search Google Scholar
    • Export Citation
  • Yang, W, Sacks, EJ, Lewis Ivey, ML, Miller, SA & Francis, DM 2005 Resistance in Lycopersicon esculentum intraspecific crosses to race T1 strains of Xanthomonas campestris pv. Vesicatoria causing bacterial spot of tomato Phytopathology. 95 5 519 527 https://doi.org/10.1094/PHYTO-95-0519

    • Search Google Scholar
    • Export Citation
  • Yang, X, Caro, M, Hutton, SF, Scott, JW, Guo, Y, Wang, X, Rashid, MH, Szinay, D, de Jong, H & Visser, RG 2014 Fine mapping of the tomato yellow leaf curl virus resistance gene Ty-2 on chromosome 11 of tomato Mol Breed. 34 2 749 760 https://doi.org/10.1007/s11032-014-0072-9

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Caleb J. Orchard Department of Horticulture and Crop Science, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691, USA

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Jonathan Kressin Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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Suchada Chompookam Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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Jutharat Chuapong Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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Namfon Onmanee Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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Karina Van Leeuwen Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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Darush Struss Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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Conrado Balatero Hortigenetics Research (South East Asia) Ltd., 7 Moo 9, Maefack Mai, Sansai, Chiang Mai 50290, Thailand

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David M. Francis Department of Horticulture and Crop Science, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691, USA

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Contributor Notes

D.M.F. is the corresponding author. E-mail: francis.77@osu.edu.

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