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J. Crop Sci. Biotech. 2010 (December) 13 (4) : 227 ~ 233 DOI No. 10.1007/s12892-010-0081-0 RESEARCH ARTICLE
Identification of QTLs for Resistance to Anthracnose to Two Colletotrichum Species in Pepper Jundae Lee1, Jee-Hwa Hong2, Jae Wahng Do1, Jae Bok Yoon1* Research and Development Unit, Pepper and Breeding Institute, Business Incubator, College of Agriculture and Life Sciences, Seoul National University, Suwon 441-853, South Korea 2 Variety Testing Division, Korean Seed & Variety Service, Ministry for Food, Agriculture, Forestry and Fisheries, Suwon 443-400, South Korea
1
Received: September 10, 2010 / Revised: November 10, 2010 / Accepted: December 9, 2010 Ⓒ Korean Society of Crop Science and Springer 2010
Abstract Pepper (Capsicum spp.) anthracnose caused by Colletotrichum spp. is a serious disease damaging pepper production in Asian monsoon regions. For QTL mapping analyses of anthracnose resistance, an introgression BC1F2 population was made by interspecific crosses between Capsicum annuum 'SP26' (susceptible recurrent parent) and Capsicum baccatum 'PBC81' (resistant donor). Both green and red fruits were inoculated with C. acutatum 'KSCa-1' and C. capsici 'ThSCc-1' isolates and the disease reactions were evaluated by disease incidence, true lesion diameter, and overall lesion diameter. On the whole, distribution of anthracnose resistance was skewed toward the resistant parent. It might indicate that one or two major QTLs are present. The introgression map consisting of 13 linkage groups with a total of 218 markers (197 AFLP and 21 SSR), covering a total length of 325 cM was constructed. Composite interval mapping analysis revealed four QTLs for resistance to 'KSCa-1' and three QTLs for 'ThSCc-1' isolate, respectively. Interestingly, the major QTLs (CaR12.2 and CcR9) for resistance to C. acutatum and C. capsici, respectively, were differently positioned but there were close links between the minor QTL CcR12.2 for C. capsici and major QTL CaR12.2 as well as the minor QTL CaR9 for C. acutatum and major QTL CcR9. These results will be helpful for marker-assisted selection and pyramiding two different anthracnose-resistant genes in commercial pepper breeding. Key words: anthracnose, Capsicum, Colletotrichum, Pepper, QTL
Introduction Pepper anthracnose, which is caused by Colletotrichum spp., is a serious disease affecting pepper production in many Asian regions including Korea, India, Indonesia, Thailand, and southern China. Colletotrichum gloeosporioides, its teleomorph Glomerella cingulata, C. acutatum, C. capsici (a synonym of C. dematium), and C. coccodes all cause pepper anthracnose (Park and Kim 1992). Among them, C. gloeosporioides has been a predominant species in South Korea for the past decade. However, the predominant species might be changing to C. acutatum (Kang et al. 2005). Colletotrichum capsici is widely distributed throughout Thailand and India (Pakdeevaraporn et al. 2005; Than et al. 2008). In nature, it occurs most often on ripe Jae Bok Yoon ( ) E-mail:
[email protected] Tel: +82-31-296-5797 / Fax: +82-31-296-5794
The Korean Society of Crop Science
(red) peppers (AVRDC 2003; Pakdeevaraporn et al. 2005), and is generally considered less aggressive than C. acutatum or C. gloeosporioides on green fruit (AVRDC 2003). Although integrated pest management for disease control is recommended, it is not easy to control anthracnose in pepper fields. Therefore, resistance breeding may be the best way to control pepper anthracnose. Despite the seriousness of pepper anthracnose, there are no resistant cultivars that are commercially produced. Several resources resistant to anthracnose have been found in other Capsicum species such as C. baccatum and C. chinense (AVRDC 1999). 'PBC80' and 'PBC81' are resistant resources in C. baccatum germplasm (AVRDC 1999; Yoon et al. 2004), and 'PBC932' is a resistant resource in C. chinense germplasm (AVRDC 2003; Pakdeevaraporn et al. 2005). These genetic resources have been used in a breeding program (AVRDC 2000; Yoon and Park 2005; Yoon et al. 2006). Anthracnose resistance in 'PBC81' has been introduced into a C.
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annuum background via both interspecific hybridization and trispecies bridge crossing (Yoon and Park 2005; Yoon et al. 2006). To overcome cross incompatibility and hybrid sterility in a cross between C. annuum and C. baccatum, embryo rescue and backcross methods, respectively, have been used (Yoon et al. 2006). The inheritance modes of anthracnose resistance to C. acutatum or C. capsici are well documented. Resistance to C. acutatum in C. baccatum 'PBC80' is inherited dominantly and quantitatively (Yoon and Park 2005), whereas resistance in C. annuum 'AR', derived from C. chinense 'PBC932', is controlled by a single recessive gene (Kim et al. 2008). Park et al. (1990) reported that resistance to C. capsici was likely inherited by partial dominance in F2 and BC populations of C. annuum 'Chungryong' x 'PI244670'. Lin et al. (2002) found that one dominant gene was responsible for resistance in C. annuum '83-168'. However, resistance in C. chinense 'PBC932' is controlled by one recessive gene, and can be affected by modifying genes (Pakdeevaraporn et al. 2005). Resistance in C. annuum 'Daepoong-cho' is also inherited recessively, and allelism tests have revealed that resistance in 'Daepoong-cho' and 'PBC932' is controlled by the same gene (Kim et al. 2008). In addition, Voorrips et al. (2004) found that resistance in C. chinense 'PRI95030' is inherited by polygenes; they applied quantitative trait locus (QTL) mapping to C. gloeosporioides and C. capsici using three resistance assessments, including infection frequency, true lesion diameter, and overall lesion diameter. One major QTL and three minor QTLs for resistance to C. gloeosporioides were detected for all three traits; whereas one major and one minor QTL for resistance to C. capsici was detected only for true lesion diameter (Voorrips et al. 2004). However, there are no reports on QTL analysis for resistance to C. acutatum and comparative analysis between resistances to C. acutatum and C. capsici in the resistant resources of Capsicum baccatum. Here we identified and compared the locations of resistant QTLs between C. capsici and C. acutatum in a BC1F2 population derived via the interspecific crossing of C. annuum x C. baccatum, and analyzed the effects of resistance assessments such as disease incidence, true lesion diameter, and overall lesion diameter on QTL analysis for pepper anthracnose.
Fig. 1. Distribution of anthracnose resistance in a BC1F2 population depending on scoring method (A and B, disease incidence; C and D, true lesion diameter; E and F, overall lesion diameter), pepper fruit stage (green or red fruits), and inoculated pathogen species (A, C, and E, C. acutatum; B, D, and F, C. capsici).
Pathogens
Materials and Methods
Colletotrichum acutatum 'KSCa-1' (abbreviated “A” below) and C. capsici 'ThSCc-1' (“C”) isolates were used. 'KSCa-1' was collected from naturally infected green or red peppers in Korean fields using the single-spore isolation method of Park and Kim (1992). 'ThSCc-1', the Thailand isolate, was obtained from S. M. Park (Seminis Thailand Co.). Inoculum preparation and incubation of post-inoculation followed the procedures of Yoon and Park (2001). The isolates were maintained on potato dextrose agar medium at 28℃ under a 16 h fluorescent light / 8 h dark cycle in an incubation chamber. The concentration of inoculum was adjusted to 5 x 105 conidia mL-1.
Plant material
Assessment of anthracnose resistance
Capsicum baccatum 'PBC81' was used as a resistant parent to C. acutatum and C. capsici, while C. annuum 'SP26' (Matikas) was used as a susceptible parent, which, based on embryo rescue, was partially compatible with 'PBC81' (Yoon et al. 2006) and was used as a recurrent parent due to hybrid male sterility. In total, 270 interspecific BC1F1 progenies [('SP26' x 'PBC81') x 'SP26'] were obtained. Among them, the highly resistant pepper '#99' was selfed to obtain BC1F2 progenies. In total, 87 individuals were planted and used for QTL mapping of anthracnose resistance.
Artificial inoculation was performed on green (abbreviated “G”) and red (“R”) fruits using the microinjection method developed by the Asian Vegetable Research and Development Center (AVRDC) (Yoon and Park 2001). Three resistance assessment methods were used (Voorrips et al. 2004): disease incidence (“D”) as a percentage of infected sites per total inoculated sites, true lesion diameter (“T”) as a mm value of infected regions among total symptom-developed sites, and overall lesion diameter (“O”) as a mm value of infected regions among total inoculated sites. A total of 12 phenotyping methods were used: ARD,
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Table 1. Descriptive statistics of anthracnose resistance according to 12 phenotyping methods in a BC1F2 population Methoda ARD AGD ART AGT ARO AGO
Mean ± SD 15.6 ± 16.9 12.1 ± 16.3 10.2 ± 9.0 13.1 ± 9.5 2.9 ± 3.8 2.6 ± 3.5
Range
Skewness
Kurtosis
Methoda
Mean ± SD
Range
Skewness
Kurtosis
0 - 73.3 0 - 85.0 0 - 29.3 0 - 28.8 0 - 20.6 0 - 15.5
1.2407 2.3226 0.3552 -0.0894 2.2518 2.1549
1.3945 6.1070 -0.7967 -1.1874 7.0617 4.6866
CRD CGD CRT CGT CRO CGO
25.1 ± 31.9 13.9 ± 18.6 6.0 ± 7.2 9.0 ± 10.9 3.2 ± 4.9 2.6 ± 4.7
0 - 100 0 - 75.3 0 - 20.0 0 - 55.0 0 - 17.9 0 - 30.0
1.1285 1.4567 0.6886 2.0752 1.5813 3.3231
0.3554 1.3051 -1.0526 6.2422 1.8054 15.0218
C, C. capsici; A, C. acutatum; R, red fruit stage; G, green fruit stage; D, disease incidence; T, true lesion diameter; O, overall lesion diameter.
a
Table 2. Correlation coefficients of anthracnose resistance between phenotyping methods in a BC1F2 population Methoda
AGD
ART
AGT
ARO
AGO
CRD
CGD
CRT
CGT
CRO
CGO
ARD AGD ART AGT ARO AGO CRD CGD CRT CGT CRO
0.470**
0.729** 0.455**
0.418** 0.553** 0.482**
0.938** 0.505** 0.760** 0.413**
0.503** 0.978** 0.474** 0.606** 0.549**
0.305* 0.138 0.457** 0.077 0.350* 0.155
0.246 0.324** 0.352** 0.314** 0.260* 0.340** 0.558**
0.249 0.170 0.393** 0.116 0.273 0.197 0.761** 0.747**
0.061 0.139 0.077 0.239* 0.082 0.148 0.401** 0.432** 0.524**
0.260 0.096 0.446** 0.048 0.325* 0.113 0.941** 0.606** 0.817** 0.445**
0.026 0.155 0.079 0.148 0.056 0.165 0.515** 0.662** 0.708** 0.714** 0.594**
C, C. capsici; A, C. acutatum; R, red fruit stage; G, green fruit stage; D, disease incidence; T, true lesion diameter; O, overall lesion diameter. and ** indicate significant differences at the 0.05 and 0.01 levels, respectively.
a
*
AGD, ART, AGT, ARO, AGO, CRD, CGD, CRT, CGT, CRO, and CGO, where, for example, ARD indicates that red (R) peppers were inoculated with the C. acutatum 'KSCa-1' (A) isolate and resistance was scored by disease incidence (D).
Simple sequence repeat (SSR) analysis In total, 232 SSR primers reported by Lee et al. (2004) and Yi et al. (2006) were synthesized by Bioneer Co., South Korea, and used in this study. DNA concentration was adjusted to 10 ng μL-1 by electrophoresis on 1.0% agarose gels and then used for PCR reactions. The PCR amplifications were performed in a 25-μL volume containing 10 ng template DNA, 10 pmol μL-1 forward and reverse primers, 2 mM MgCl 2, 0.25 μM of each dNTP, 10x buffer solution, and 1 unit Taq polymerase (Takara, Japan). All primer combinations consisted of a 4 min initial denaturation at 94℃ followed by 30 or 35 PCR cycles of 30 s at 94℃, 1 min at 50℃, 55℃, or 60℃, 2 min at 72℃, and a final 10min extension at 72℃ on a programmable thermal cycler (model T1 thermocycler, Biometra Co., Germany). PCR products were separated on denatured 5% polyacrylamide gels, and then silver stained using a Silverstar Staining Kit (Bioneer, South Korea) according to the manufacturer's instructions. The SSRs were scored codominantly.
Amplified fragment length polymorphism (AFLP) analysis AFLP analysis was applied as described by Vos et al. (1995). Polymorphic markers were detected using combinations of EcoRI and MseI. The pre-selective amplification cycle was performed with one selective nucleotide (E-A/M-G and E-T/M-C), followed by a selective amplification cycle with two additional selective nucleotides. We used a total of 38 primer combinations.
Linkage mapping Linkage maps were constructed using the software Mapmaker/EXP v. 3.0 (Lincoln et al. 1993). Distorted polymorphic markers were excluded by chi-squared tests (P < 0.001), and identical markers were eliminated. Linkage groups were divided by LOD 4.0 and a maximum distance of 30 cM. The mapping function of Kosambi (1944) was used. Linkage maps were drawn using MAPCHART v. 2.1 (Voorrips 2002).
QTL analysis Composite interval mapping (CIM) was used to map the QTLs controlling anthracnose resistance using the software package Windows QTL Cartographer v. 2.5 (Wang et al. 2007). CIM was run at a 2 cM walk speed using the parameters of model 6, five control markers, a 10 cM window size, and the forward and backward method in the program. The significance threshold level was defined as the 50th highest LOD value by running 1,000 permutations.
Results Distribution of anthracnose resistance Anthracnose resistance was evaluated using 12 phenotyping methods in 87 individuals of a BC1F2 population. The distributions of resistance are shown in Fig. 1. On the whole, resistance was skewed toward the resistant parent. Skewness of AGD, ARO, AGO, CGT, and CGO was more than 2.0 (Table 1). The ranges of resistance were 0 - 100%, 0 - 55 mm, and 0 - 30 mm for disease incidence, true lesion diameter, and overall lesion diameter, respectively (Table 1). The distribution patterns of dis-
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QTL Analysis for Pepper Anthracnose Resistance
ease incidence were highly similar to those of overall lesion diameter but not true lesion diameter (Fig. 1). The correlation coefficients of 0.938 between ARD and ARO, 0.978 between AGD and AGO, and 0.941 between CRD and CRO were higher than those of 0.729 between ARD and ART, 0.760 between ARO and ART, 0.553 between AGD and AGT, 0.606 between AGO and AGT, 0.761 between CRD and CRT, and 0.817 between CRO and CRT (Table 2). Resistance scored by true lesion diameter was more evenly distributed than that scored by disease incidence and overall lesion diameter except for CGT (Fig. 1). The kurtosis of ART, AGT, and CRT was lower than 0 (Table 1). Resistance correlations within C. acutatum or C. capsici inoculation were higher than those between C. acutatum and C. capsici inoculations except for ART and CGD (Table 2). ART was highly correlated with all C. acutatum data as well as CRD, CGD, CRT, and CRO, while CGD was also highly correlated with all C. capsici and C. acutatum data except ARD (Table 2).
Table 3. Summary of the linkage map made in an introgressed BC1F2 population Linkage Length The number group (cM) of markers LG1-1 LG1-2 LG4 LG6 LG7-1 LG7-2 LG9 LG10 LG11 LG12 LGA LGB LGC Total
19 11 10 40 22 1 16 6 76 43 35 27 19 325
19 11 10 40 22 1 16 6 76 43 35 27 19 325
SSR markera
QTL-detected trait
CAN10950, HpmsE014 Hpms1-148 HpmsAT2-14, HpmsE006 HpmsE072, HpmsE059, AF208834 HpmsE020, HpmsE038 -b Hpms2-24, HpmsE143 Hpms2-21 HpmsE012, HpmsE046 HpmsE092, HpmsE032, HpmsE063 -
CGD, CRT, CRO ART, AGT CRD -
a
SSR markers were originally reported in Lee et al. (2004) and Yi et al. (2006). - means none.
b
Linkage map A total of 375 markers including 340 AFLPs and 35 SSRs were scored after polyacrylamide gel electrophoresis and silver staining, and used for linkage mapping analysis. A total of 102 distorted markers were excluded via the chi-squared test (P < 0.001), and 17 identical markers were eliminated. Finally, 256 markers were used for linkage grouping, and 218 markers (197 AFLPs and 21 SSRs) were mapped (Table 3 and Fig. 2). Thirteen linkage groups were constructed, covering a total length of 325 cM, with an average distance of 1.49 cM between adjacent markers (Table 3 and Fig. 2). Based on the linked SSR markers, LG 1, 4, 6, 7, 9, 10, 11, and 12 were named after the linkage groups previously reported by Lee et al. (2004) and Yi et al. (2006), and the remaining linkage groups were assigned to LG A, B, and C in the order of linkage group length (Table 3 and Fig. 2).
QTL analysis CIM analysis revealed two significant QTLs for resistance to C. acutatum and C. capsici, respectively (Table 4). CaR12.1 and CaR12.2 (C. acutatum resistance loci on LG12) were detected in ART and AGT (Table 4 and Fig. 3). The CaR12.2 located between the EtatMcgc04d and EataMcgc01 (interval of 8.1 cM) markers was a main-effect QTL, which explained 20.46 and 11.90% of phenotypic variance (PVE) of ART and AGT, respectively (Table 4). The AFLP marker EataMcgc01 was the closest to CaR12.2 (Fig. 3). The minor QTL CaR12.1 was detected in only ART with a 17.92% PVE value, and it was positioned between the EtagMcag11 and EtccMcga05 markers (Table 4). CcR9 and CcRC were detected as resistant QTLs to C. capsici (Table 4 and Fig. 4). The CcR9 was a main-effect QTL, which was located between HpmsE143 and EtgaMccg10, and had >50% PVE values in CGD, CRT, and CRO (Table 4 and Fig. 4). The EtgtMcgt03 was the closest marker to CcR9 (Fig. 4). Interestingly, CcRC was a minor QTL that originated from C. annuum 'SP26', which was a susceptible parent (Table 4).
Fig. 3. LOD profiles for main-effect QTLs resistant to C. acutatum on linkage group 12. Boxes: C, C. capsici; A, C. acutatum; R, red fruit stage; G, green fruit stage; D, disease incidence; T, true lesion diameter; O, overall lesion diameter. Arrows: QTL peaks over LOD threshold.
Fig. 4. LOD profiles for main-effect QTLs resistant to C. capsici on linkage group 9. Boxes: C, C. capsici; A, C. acutatum; R, red fruit stage; G, green fruit stage; D, disease incidence; T, true lesion diameter; O, overall lesion diameter. Arrow: QTL peak over LOD threshold.
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Fig. 2. Linkage maps in an introgressed BC1F2 population using a total of 218 markers including 197 AFLPs and 21 SSRs. Names of LG 1, 4, 6, 7, 9, 10, 11, and 12 were based on the linked SSR markers previously reported by Lee et al. (2004) and Yi et al. (2006). The names of LG A-C were classified by linkage group length. Map distance (cM) calculated by the Kosambi function is located on the left side of the vertical bars; marker names are to the right.
Table 4. Main-effect QTLs detected by composite interval mapping (CIM) analysis for anthracnose resistance in a BC1F2 population Methoda ART ART AGT CRD CGD CRT CRO
LG
QTLb
Flanking marker
Position (cM)
Interval (cM)
LOD
Ac
Dd
|D/A|
r2 (%)e
LOD threshold (95%)
12 12 12 C 9 9 9
CaR12.1 CaR12.2 CaR12.2 CcRC CcR9 CcR9 CcR9
EtagMcag11-EtccMcga05 EtatMcgc04d-EataMcgc01 EtatMcgc04d-EataMcgc01 EaacMcgc02-EaatMccg07 HpmsE143- EtgtMcgt03 HpmsE143- EtgtMcgt03 EtgtMcgt03-EtgaMccg10
6.1 15.9 13.9 12.1 10.0 10.0 10.6
1.0 8.1 8.1 7.1 2.6 2.6 3.2
4.74 9.57 7.83 6.71 13.36 15.98 13.94
5.72*** 5.88*** 4.84*** -16.6 27.66 14.10** 11.41**
-0.08 1.66 5.78 -45.2*** -15.09*** -8.95*** -8.10***
0.02 0.28 1.19 2.72 0.55 0.63 0.71
17.92 20.46 11.90 10.59 57.48 78.91 76.75
3.84 3.84 4.08 6.12 11.42 9.18 8.03
P < 0.05; ** P < 0.01; *** P < 0.001. C, C. capsici; A, C. acutatum; R, red fruit stage; G, green fruit stage; D, disease incidence; T, true lesion diameter; O, overall lesion diameter. b CaR, resistant loci to C. acutatum; CcR, resistant loci to C. capsici. c A, additive effect. d D, dominant effect. e 2 r , phenotypic variance explained (PVE). * a
Discussion Using QTL analysis for pepper anthracnose resistance, we identified three QTLs for C. acutatum and four QTLs for C.
capsici (Tables 3 and 4). The major QTL (CaR12.2) resistant to C. acutatum was different from the major QTL (CcR9) for C. capsici resistance (Figs. 3 and 4), suggesting that pepper has different resistance genes according to the species of anthracnose pathogen. However, Voorrips et al. (2004) reported that the
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QTL Analysis for Pepper Anthracnose Resistance
main QTL (B1) was resistant to C. gloeosporioides as well as C. capsici. This major QTL B1 might be the same as the major QTL CcR9 of the present study (Fig. 4). To verify this, it would be necessary to demonstrate that the SSR marker CA-MS12 closely linked to B1 was positioned in this linkage map. Interestingly, the minor QTL CcR12.2 and the major QTL CaR12.2 were located at the same position, while the minor QTL CaR9 and the major QTL CcR9 were positioned at the same site (Table 4; Figs. 3 and 4). Because ART was significantly correlated with CRD, CGD, CRT, and CRO (Table 2), the minor QTL CaR9 might be detected in ART (Table 4). Similarly, the minor QTL CcR12.2 could be found in CGD (Table 4) because CGD was significantly correlated with all C. acutatum data except for ARD (Table 2). No QTLs were detected using >2.0 skewness (Table 1). Pakdeevaraporn et al. (2005) reported that resistance of C. chinense PBC932 to C. capsici was inherited recessively. However, we found that the dominance/additive ratio (d/a) of the major QTL CcR9 was 0.55 - 0.71 (Table 4), indicating that the mode of gene action is partial dominance. This difference in resistance inheritance might result from resistant resources, such as C. baccatum 'PBC81' in this study and C. chinense 'PBC932' in the study by Pakdeevaraporn et al. (2005). Voorrips et al. (2004) reported that the resistant parent carried a susceptible allele for resistant QTLs to C. gloeosporioides (B2) as well as C. capsici (G1). Similarly, resistant alleles of CaR7 and CcRC QTLs were found in a susceptible parent (C. annuum 'SP26') in the present study (Table 4). Correlation analysis revealed that scoring results by true lesion diameter (TLD) differed slightly from the other methods (disease incidence, DI, and overall lesion diameter, OLD; Table 2). DI was highly similar to OLD (correlation coefficients >0.93; Fig. 1 and Table 2), because TLD focused on growth when diseased whereas DI and OLD emphasized the occurrence of disease. Recently, Lee et al. (2009) reported that the total length of pepper integrated genetic map is 2,143 cM. In this study, however, the total length of linkage map is so short (only 325 cM) because we used the introgressed BC1F2 population selfed from one BC1F1 plant ('#99') highly resistant to C. acutatum and C. capsici and because an interspecific cross between C. annuum and C. baccatum induced interspecific incompatibility and hybrid sterility (Yoon et al. 2006). To use QTL-linked markers for marker-assisted selection (MAS), closely linked and flanked markers are needed. Because the interval length (8.1 cM) of CaR12.2 was substantially wide, fine mapping will be needed to further saturate the map in this region. An AFLP marker, EataMcgc01, the closest marker to CaR12.2, will need to be converted into simple codominant PCR markers. An SSR marker, HpmsE143, and two AFLP markers, EtgtMcgt03 and EtgaMccg10, closely linked markers flanking CcR9, will also need to be converted into breeder-friendly markers. These markers will be useful for MAS to develop anthracnose-resistant strains and to pyramid two different anthracnoseresistant genes in commercial pepper breeding.
Acknowledgments This work was partially supported by a grant (#20050301034 408) from the BioGreen 21 Program and by a grant (#20100401 086013001) from the Agricultural R&D 15 Agendas, Rural Development Administration, Republic of Korea.
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