Polygenic segregation of BW resistance in the hybrid population
BW resistance is controlled by multiple genes in potato plants (Elphinstone 1994; Rowe and Sequeira 1970; Sequeira 1979) and is greatly influenced by environmental conditions such as temperature and soil moisture (Tung et al. 1990a, b). Different strains show resistance to different extents (French and De Lindo 1982; Katayama and Kimura 1984; Tung et al. 1990a; Suga et al. 2013). Thus, the resistance was evaluated against three strains using an in vitro assay method (Habe 2018) under controlled environmental conditions at 24°C and 28°C. The RP and SP plants showed stable resistance and susceptibility against all the strains used, including phylotype I/biovar 3, phylotype I/biovar 4, and phylotype IV/biovar 2A. The resistance levels in the hybrid population varied consistently, confirming that the resistance was polygenically controlled, and the resistance was positively correlated among all six treatments, indicating that the pathogenicity was similar between phylotypes I and IV in potato plants. This was in agreement with previous findings that indicate no difference in virulence between phylotypes I and IV and between phylotypes II and III in potato cultivars (Habe et al. 2016; Sharma et al. 2021). Although Suga et al. (2013) reported that phylotype IV is more virulent than phylotype I, the classification of phylotypes may not correlate with the degree of virulence as suggested for tomato, eggplant, and pepper plants (Lebeau et al. 2011).
Segregation of multiple resistance QTLs in the hybrid population
CIM and non-parametric QTL mapping were performed to evaluate BW resistance using a hybrid population, which identified five major QTLs (qBWR-3, qBWR-6a, qBWR-6b, qBWR-7, and qBWR-10b) and five minor QTLs (qBWR-1a, qBWR-1b, qBWR-5, qBWR-10a, and qBWR-11). Only QTLs conferring heterozygous resistance in either one of the parents could be segregated and mapped in the population. Thus, the ten QTLs were likely the minimal ones that could be detected using this population. The combined segregation resulted in transgressive segregation, where hybrid plants with higher levels of resistance than that in RP and those with lower levels of susceptibility than that in SP were obtained. The resistance-related QTL alleles were derived from both parents.
Resistance specificity to strains and temperatures
We found strain-specific and temperature-dependent QTLs (qBWR-6a, qBWR-6b, and qBWR-10b) and strain-non-specific and broad-spectrum resistance QTLs (qBWR-3 and qBWR-7). qBWR-6a, qBWR-6b, and qBWR-10b considerably contributed to the resistance to MAFF327142 (phylotype I/biovar 3), in which the latter two were more effective at 24°C. The distributions of the DIs in the F1 population were skewed toward relatively lower DIs at 24°C and toward higher DIs at 28°C, which was likely due to the effect of qBWR-6b (Fig. 1ab). qBWR-6b was considered to be derived from RP 10-03-30, a haploid clone of Saikai 35 (Habe et al. 2019), which was originally derived from S. phureja (Mori et al. 2012). S. phureja is a well-known source of BW-resistant factors, and the resistance is strain-specific and sensitive to high temperatures (Sequeira and Rowe 1969; Sequeira 1979; Ciampi and Sequeira 1980; French and De Lindo 1982). The strain-specific resistance of S. phureja appeared to be simply inherited in few cases (Elphinstone 1994). Therefore, we suggest that qBWR-6b was derived from S. phureja and functions as a simply-inherited, major QTL at low temperatures. qBWR-3 and qBWR-7 showed stable resistance to all strains at low and high temperatures, irrespective of different phylotypes and biovars. These QTLs may be effective under diverse environmental conditions and highly desired in breeding BW-resistant cultivars.
Reliability of the BW resistance QTLs
Chen et al. (2013) identified S. chacoense-derived BW resistance QTLs against the race 1/biovar 3 strain on chromosomes 2 and 9. The SP used in our study was F1-1, an interspecific hybrid between S. chacoense and S. phureja (Hosaka and Hanneman 1998). However, we did not identify any QTLs on chromosomes 2 and 9, indicating that the source of resistance factors for all the QTLs detected in our study was S. phureja. In our previous study using the same F1 population and the same inoculum (MAFF327001, phylotype I/ biovar 4) at 28°C, five QTLs were identified on chromosomes 1, 3, 7, 10, and 11 (Habe et al. 2019). When their locations were compared, the previously identified QTLs qBWR-1, qBWR-2, qBWR-3, qBWR-4, and qBWR-5 correspond to the QTLs identified in the present study: qBWR-1b, qBWR-3, qBWR-7, qBWR-10a, and qBWR-11, respectively. The QTL qBWR-5 on chromosome 5 which showed a minor contribution to resistance was newly found, and qBWR-11 was not significant in this study (Table 1). Repeated resistance assays may increase or decrease certain genetic variances, affecting significance levels of the QTLs. Here, difficulty in the BW resistance evaluation was featured again, and importance of the major-effect QTLs is emphasized.
Universal resistance QTLs
BW resistance QTLs have been identified in chromosomes 3, 4, 6, 8, 10, 11, and 12 in tomato plants (Thoquet et al. 1996a, 1996b; Mangin et al. 1999; Carmeille et al. 2006; Wang et al. 2000, 2013) and in chromosomes 1, 2, 3, 4, 5, 6, 7, 8, and 9 in eggplants (Mimura et al. 2012; Lebeau et al. 2013; Salgon et al. 2017, 2018). Comparison of the physical location in each chromosome indicates that the strain-specific resistance QTL qBWR-6b is likely to be colocalized with tomato QTL (Bwr-6) and eggplant QTL (ERPR6) on chromosome 6 (Fig. 3b). However, both Bwr-6 and ERPR6 confer resistance against phylotypes І and ІІ (Carmeille et al. 2006; Wang et al. 2013; Salgon et al. 2018; Shin et al. 2020), whereas the resistance of qBWR-6b is limited to phylotype I/biovar 3. The mapping position of Bwr-6 slightly varies depending on different inoculums and field conditions (Wang et al. 2013), which was similarly observed for ERPR6 (Salgon et al. 2018). These findings indicate that strain-specific single-locus resistance genes are clustered on the same chromosome (Meyers et al. 1998; Andolfo et al. 2013), which superficially made Bwr-6 and ERPR6 broad-spectrum resistance genes (Salgon et al. 2018). For Bwr-6 in tomato, 18 candidate genes have been proposed (Kim et al. 2018; Shin et al. 2020; Abebe et al. 2020).
A tomato-derived QTL (Bwr-3) and two eggplant-derived QTLs (ERPR3a and ERPR3b) have been reported on chromosome 3 (Thoquet et al. 1996b; Carmeille et al. 2006; Wang et al. 2013; Salgon et al. 2018). Bwr-3 and ERPR3b are colocalized and may include the same locus (Salgon et al. 2018), while the potato-derived QTL qBWR-3 is likely colocalized with ERPR3a (Fig. 3a). Like qBWR-3, ERPR3a is a strain-non-specific, broad-spectrum QTL (Salgon et al. 2018). The nearest SNP locus to qBWR-3 (solcap_snp_c2_50637) is located in the receptor-like kinase gene (PGSC0003DMG400016685). This gene may represent one of candidate genes for BW resistance because a leucine-rich repeat receptor-like kinase gene (ERECTA) is involved in BW resistance in Arabidopsis thaliana (Godiard et al. 2003).
The broad-spectrum resistance QTL qBWR-7 was detected in a span between 12.2 and 27.2 cM or between 10.9 and 39.2 Mb near the centromere, where recombination is less likely to occur, and comprised 23 SNP loci at the peak position (25.3 cM) (Table 1). The long arm of chromosome 7 in potato plants harbors a resistance gene hotspot containing Rpi1 and Rpi2 against Phytophthora infestans and Gro1-4 against Globodera rostochiensis (Ballvora et al. 1995; Kuhl et al. 2001; Paal et al. 2004; Ruggieri et al. 2014; Yan et al. 2017); however, qBWR-7 is considered to be excluded in this hot spot. Since the effect of resistance of qBWR-7 is slightly higher than that of qBWR-3, additional fine mapping is desired to determine the accurate location and to develop molecular markers.