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Barka and Lee: Molecular Marker Development and Gene Cloning for Diverse Disease Resistance in Pepper (Capsicum annuum L.): Current Status and Prospects

Abstract

The production of chili pepper (Capsicum annuum L.) is hindered by several biotic factors even though striding progresses were made in genetic improvement in the last two decades. Among the advancements were the fast-track genetic improvement of disease-resistant varieties by the use of marker-assisted selection (MAS) and the conventional breeding-based introgression of major resistance genes. Marker development, marker-based identification and fine mapping have revealed a large number of resistance genes, from which cloning of some candidate genes demonstrated the applicability and versatility of map-based cloning for disease resistance. In some of the recent fine mapping of disease resistance QTLs, closely linked DNA markers were identified, which in turn resulted in the rapid introgression of target gene(s) into breeding lines. Also, progresses were made on the characterization and map-based cloning of resistance genes conferring broad-spectrum resistance. As the number of identified and characterized resistance genes and the DNA markers linked to resistance genes are steadily generated, the development of multiple/durable resistance to major chili pepper diseases is accelerated by MAS. In the present review, the development of molecular markers, marker-based mapping of genes conferring resistance to ten major chili pepper diseases were discussed, focusing on the recent advancements in major and QTL-spanning resistance gene mapping. The review provides up-to-date insights into the development of DNA markers linked to disease resistance genes and the cloning of resistance genes, which are all so crucial in pepper breeding for disease resistance.

INTRODUCTION

Chili pepper (Capsicum annuum L.) is among the top economically valuable vegetable crops mainly due to the high demand and popularity of spicy foods in many parts of the world (Pinto et al. 2016). However, the production of pepper is hindered by diverse diseases including fungal (anthracnose and powdery mildew), oomycete (phytophthora root rot), viral (Cucumber mosaic virus [CMV], tobamoviruses, potyviruses, Tomato spotted wilt virus [TSWV], etc.), bacterial (bacterial spot and bacterial wilt) and nematode (root-knot nematodes) (Barchenger et al. 2019). Therefore, pepper breeding for multiple resistances to diverse diseases is highly required (Wiesner-Hanks and Nelson 2016). It can be achieved by the fast-track accumulation of disease resistance genes through the use of marker-assisted selection (MAS) (Ribaut and Hoisington 1998; Cobb et al. 2019). Recently, the rapid detection of single nucleotide polymorphism (SNP) markers associated with disease resistance genes by the high-throughput genotyping methods combined with the next-generation sequencing (NGS) technologies has substantially shortened the time required for genetic map construction, quantitative trait loci (QTL) analysis and candidate gene identification in plant molecular breeding (Rafalski 2002; Varshney et al. 2009; Kumar et al. 2012; Mammadov et al. 2012; Thomson 2014; Huq et al. 2016; Phan and Sim 2017; Xu et al. 2017). The frequently adopted methods for high-throughput SNP genotyping include genotyping-by-sequencing (GBS) (Deschamps et al. 2012; Poland and Rife 2012; Kim et al. 2016), double-digest restriction association DNA sequencing (ddRAD-seq) (Peterson et al. 2012), and specific-locus amplified fragment sequencing (SLAF-seq) (Sun et al. 2013). Molecular marker development and fine mapping for disease resistance genes and the eventual identification and characterization of such genes by map-based cloning are believed to bring a paradigm shift in the speed of disease-resistant pepper variety development.
The aim of the present review was to discuss some of the latest advancements in marker development and gene cloning for major disease resistances in chili pepper. The review could also be used as an important input for such molecular breeding programs involving MAS, as it highlighted some of the latest reports on the identification of candidate disease resistance genes and associated/tightly-linked DNA markers.

MARKER DEVELOPMENT FOR PEPPER DISEASE RESISTANCE

Anthracnose

Pepper anthracnose is characterized by water-soaked and sunken circular lesions on mature/immature fruits caused by Colletotrichum species including C. scovillei (formerly C. acutatum), C. truncatum (formerly C. capsici), and C. siamense (formerly C. gloeosporioides) (Mongkolporn and Taylor 2018). It has been reported that some genetic resources belonging to two Capsicum species, C. baccatum (‘PBC80’, ‘PBC81’, ‘PI594137’, and ‘Cbp’) and C. chinense Jacq. (‘PBC932’), have resistance to anthracnose (AVRDC 2003; Yoon et al. 2004; Kim et al. 2008e; Park et al. 2009). The DNA markers linked to anthracnose resistance in Capsicum species were summarized in Table 1.
The resistances of C. annuum ‘AR’ derived from C. chinense ‘PBC932’ and C. baccatum ‘PI594137’ to C. scovillei were reported to be controlled by a single recessive gene and a single dominant gene, respectively, through inheritance analysis (Kim et al. 2007, 2008d). In another study, the resistance of C. baccatum ‘PBC80’ to C. scovillei was controlled by two genes, co4 and Co5, based on phenotypic data (Mahasuk et al. 2009b). Two QTLs, An8.1 and An9.1, for resistance to C. scovillei were detected in an F2 population derived from a cross between C. baccatum var. pendulum (‘Cpb’) (resistant) and C. baccatum ‘Golden-aji’ (susceptible) (Kim et al. 2010). A major QTL CaR12.2 for the resistance was found in an introgressed BC1F2 population by interspecific crosses between C. annuum ‘SP26’ (susceptible) and C. baccatum ‘PBC81’ (resistant), and so was the development of CaR12.2M1-CAPS marker closely linked to the major QTL CaR12.2 (Lee et al. 2010, 2011). Another QTL analysis revealed that the resistance of C. chinense ‘PBC932’ to C. scovillei is controlled by a major dominant QTL on chromosome P5 (Sun et al. 2015). Recently, three major (RA80rP2, RA80rP3.1, and RA80rHP1) and two minor (RA80rP3.2 and PA80rHP2) QTLs for resistance to C. scovillei in the ripe fruit stage were identified in an F2 population derived from an intraspecific cross between C. baccatum ‘PBC80’ and ‘CA1316’ (Mahasuk et al. 2016). Two markers, SCAR-Indel and SSR-HpmsE032, associated with resistance to C. scovillei were validated in two C. annuum anthracnose resistant introgression lines, PR1 derived from ‘PBC932’ and PR2 derived from ‘PBC80’, resulted in the selection efficiency of 77% when both markers were used together (Suwor et al. 2017).
QTL analysis for resistance to C. siamense and C. truncatum in a cross between C. annuum ‘Jatilaba’ (susceptible) and C. chinense ‘PRI95030’ (resistant) revealed one main QTL (B1) and three other QTLs (B2, H1, and D1) for the resistance (Voorrips et al. 2004). Inheritance analysis indicated that the resistance of ‘PBC932’ to C. truncatum was responsible by a single recessive gene (Pakdeevaraporn et al. 2005; Kim et al. 2008d). Three different recessive genes, co1, co2, and co3, were responsible for the resistance to C. truncatum of green fruit, red fruit, and seedling, respectively, from a cross between C. annuum ‘Bangchang’ and C. chinense ‘PBC932’, and two QTLs RA932g (co1) and RA932r (co2) were detected in the same population (Mahasuk et al. 2009a, 2016). A major QTL CcR9 for the resistance of ‘PBC81’ to C. truncatum was identified, and the CcR9M1-SCAR marker closely linked to the QTL CcR9 was developed (Lee et al. 2010, 2011). An SSR marker HpmsE032 was associated with resistance in progressive lines derived from ‘PBC80’ to C. truncatum at green fruit stages and could be considered useful in the selection of resistance derived from ‘PBC80’ (Suwor et al. 2015). Recently, reference genome sequences of C. baccatum and QTL information for resistance to C. truncatum revealed 64 nucleotide-binding and leucine-rich-repeat proteins (NLRs) from a 3.8 Mb region of chromosome 3 as candidate resistance genes for C. truncatum (Kim et al. 2017b). Bulked segregant analysis (BSA) combined with inter-simple sequence repeat (ISSR) and amplified fragment length polymorphism (AFLP) markers has resulted in the development of two sequence-tagged site (STS) markers (CtR-431 and CtR-594) linked to the resistance (RCt1) locus against C. truncatum in C. annuum (Mishra et al. 2019).

Powdery mildew

Powdery mildew, caused by Leveillula taurica, anamorph Oidiopsis taurica, is a serious disease of pepper (C. annuum) grown in greenhouses (de Souza and Café-Filho 2003). The symptoms are characterized by a powdery-white fungal growth on the undersides of leaves and light-green to yellow blotches on the upper leaf surfaces (de Souza and Café-Filho 2003). Nine resistant resources to powdery mildew, including three C. annuum accessions (H3, H-V-12 and 4648) and six C. baccatum accessions (CNPH 36, 38, 50, 52, 279 and 288), were identified after evaluating a total of 162 Capsicum genotypes (Daubeze et al. 1995; de Souza and Café-Filho 2003). There are several reports on the development of molecular markers for powdery mildew resistance in Capsicum species (Table 1).
The resistance to powdery mildew from an African pepper line ‘H3’ (C. annuum) was controlled by two or three genetic factors with additive and partial dominance effects (Daubeze et al. 1995). Two common QTLs, Lt_6.1 (a closely linked AFLP maker E36/M59-380h) and Lt_9.1 (a closely linked random amplified polymorphic DNA [RAPD] marker D11_0.8h), for resistance to powdery mildew under natural and artificial infections were detected in the doubled haploid (DH) progeny from the cross between ‘H3’ (highly resistant) and ‘Vania’ (susceptible) (Lefebvre et al. 2003). Recently, a novel powdery mildew resistance locus, PMR1, and cosegregating markers, one sequence characterized amplified region (SCAR) marker (ZL1_1826) and five high-resolution melting (HRM) (Liew et al. 2004) markers (HPGV_1313, HPGV_1344, HPGV_ 1412, KS16052G01, and HRM2_A4), were identified on pepper chromosome 4 using two populations, 102 ‘VK515’ F2:3 families and 80 ‘PM Singang’ F2 plants (Jo et al. 2017). In addition to that, the report indicated that PMR1 locus might have been introgressed from C. baccatum.

Phytophthora root rot

Phytophthora capsici is one of the destructive pathogens posing a serious threat to vegetables and fruits including chili pepper (C. annuum). Several resistant resources to Phytophthora root rot, including C. annuum ‘Vania’, ‘Perennial’, ‘Criollo de Morelos 334 (CM334)’, ‘CM331’, ‘AC2258’, ‘YCM334’, ‘PI201234’, ‘PBC280’, ‘PBC495’, and ‘PBC602’, have been reported (Lee et al. 2012b). In pepper, resistance to P. capsici is attributed to single dominant gene (Monroy-Barbosa and Bosland 2008) and the joint action of hundreds of the most diversified partial resistance QTLs (Truong et al. 2012). The list of QTLs and DNA markers associated with the resistance is shown in Table 2.
Comparative QTL analysis for resistance to Phytophthora capsici was performed in three intraspecific pepper populations derived from three different resistant accessions, C. annuum ‘Vania’, ‘Perennial’, and ‘CM334’, and the major resistance factor on chromosome P5 was found to be common to the populations (Thabuis et al. 2003). Moreover, resistance alleles to P. capsici at four QTLs were transferred from a small-fruited pepper into a bell pepper using four markers, ASC031 (P2), ASC037 (P5), E43M53-159y (P5), and E35M61-114y (P10) (Thabuis et al. 2004). The D4 SCAR marker for the detection of Phyto.5.2, a major QTL for resistance to P. capsici, was developed (Quirin et al. 2005). In another study, two intraspecific linkage maps, ‘PSP-11’ × ‘PI201234’ and ‘Joe E. Parker’ × ‘CM334’, were constructed to identify QTLs conferring resistance to P. capsici root-rot and foliar-blight diseases (Ogundiwin et al. 2005). Three QTLs, Phyt-1, Phyt-2, and Phyt-3, for resistance to Phytophthora blight, were detected using an intraspecific DH population derived from a cross between C. annuum ‘K9-11’ (susceptible) and ‘AC2258’ (resistant), and three markers, M10E3-6 AFLP, RP13-1 RAPD, and M9E3-11, for the QTLs, respectively, were identified (Sugita et al. 2006). Two markers, CAMS420 SSR (linked to a major QTL on LG15) and CTT/ACT3M AFLP (a minor QTL on LG3), for resistance to P. capsici were identified in a segregating DH population developed by anther culture of an F1 plant crossed between C. annuum ‘Manganji’ (susceptible) and ‘CM334’ (resistant) (Minamiyama et al. 2007). Two bacterial artificial chromosome (BAC)-derived markers, P5-SNAP and SSR-9, were developed from two RFLP markers, CDI25 (P5) and CT211 (P9), linked to P. capsici resistance which were detected in an F2 population from a cross between C. annuum ‘CM334’ (resistant) and ‘Chilsungcho’ (susceptible) (Kim et al. 2008b). The M3-CAPS marker tightly linked to the major QTL Phyto.5.2 for resistance to Phytophthora root rot, was developed using two segregating F2 populations from a cross of ‘Subicho’ × ‘CM334’ and self-pollination of a commercial cultivar ‘Dokyacheongcheong’ (Lee et al. 2012b). One common QTL (P5) and four isolate-specific QTLs (P10, P11, Pb, and Pc) for resistance to Phytophthora root rot were detected using two P. capsici isolates (09-051 and 07-127) and an intraspecific recombinant inbred line (RIL) population from a cross between ‘YCM334’ (resistant) and ‘Tean’ (susceptible) (Truong et al. 2012). Subsequently, a codominant SCAR marker SA133_4 and a RAPD marker UBC553, linked to the QTL P5, were developed (Truong et al. 2013). By means of meta-analyses, a key QTL, Pc5.1, conferring broad-spectrum resistance to P. capsici was identified (Mallard et al. 2013). A resistance gene, C. annuum DOWNY MILDEW RESISTANT 1 (CaDMR1), as a candidate gene responsible for the major QTL on chromosome P5 for resistance to P. capsici was identified by generating a high-density map with 3887 markers in a set of RIL derived from the highly resistant C. annuum ‘CM334’ and the susceptible ‘Early Jalapeno’ (Rehrig et al. 2014). The Phyto5NBS1, a reliable marker for P. capsici resistance, was developed using BSA and Affymetrix GeneChips (Liu et al. 2014). A single dominant gene, PhR10, mapped on chromosome 10, was identified to be responsible for the resistance of ‘CM334’ to an isolate Byl4 (race 3) of P. capsici using BSA and SLAF-seq, and two flanking SSR markers, P52-11-21 and P52-11-41, of the PhR10 locus were also identified (Xu et al. 2016). Two candidate genes, Capana05g000764 and Capana05g000769, for a dominant gene CaPhyto controlling the resistance of ‘PI201234’ to P. capsici race 2, were identified, and one SSR marker, ZL6726, most closely linked to CaPhyto at a distance of 1.5 cM, was developed (Wang et al. 2016). Through GBS-based QTL mapping and GWAS analysis, three major QTLs (5.1, 5.2, and 5.3) conferring broad-spectrum resistance to P. capsici were identified (Siddique et al. 2019).

Cucumber mosaic virus

Cucumber mosaic virus (CMV), a member of the Cucumovirus genus in the family Bromoviridae, is a plant RNA virus which often causes significant losses in dicots including pepper and some monocot crops due to the rapid spread of the disease by aphids, and other vectors (Roossinck 2001). Up to date, CMV resistance has been identified in various genetic sources of pepper (Capsicum spp.) including C. annuum ‘Perennial’ (Lapidot et al. 1997), ‘Vania’ (Caranta et al. 2002), ‘Sapporo-oonaga’ and ‘Nanbu-oonaga’ (Suzuki et al. 2003), ‘Bukang’ (Kang et al. 2010), ‘BJ0747-1-3-1-1’ (Yao et al. 2013), ‘CA23’ (Rahman et al. 2016), C. frutescens ‘BG2814-6’ (Grube et al. 2000b), ‘Tabasco’, ‘LS1839-2-4’ (Suzuki et al. 2003), ‘PBC688’ (Guo et al. 2017a), and C. baccatum ‘PI439381-1-3’ (Suzuki et al. 2003).
Several researches on CMV resistance in Capsicum species have been reported (Table 3). The resistance of these resources was reported to be quantitatively controlled. Two additive QTLs on LG3 and Noir and one epistatic QTL between TG124 (positioned on Noir) and TG66 (positioned on Pourpre) were identified using 94 DH lines obtained from the F1 of the ‘Perennial’ and ‘Yolo Wonder’ parental varieties (Caranta et al. 1997b). In the same population, the major QTL for CMV resistance was positioned on chromosome 12, with an R2 (coefficient of determination) of 19% and a strong linkage with the A5.1 marker (Pflieger et al. 1999). Also, four QTLs, cmv4.1, cmv6.1, cmv11.1, and cmv13.1, were detected using 180 F3 families derived from a cross between C. annuum ‘Maor’ and ‘Perennial’ (Ben Chaim et al. 2001).Among them, QTL cmv11.1 was detected in all the experiments (Volcani 97, 98, and Cornell 97) and had the largest R2 values (16-33%) (Ben Chaim et al. 2001).Four QTLs, cmv5.1, cmv11.1, cmv11.2, and cmv12.1, which involved the partial restriction of long-distance CMV movement, were mapped in a DH population derived from the F1 hybrid between C. annuum ‘H3’ and ‘Vania’ (Caranta et al. 2002). The major-effect QTL cmv12.1, detected in two separate experiments using the CMVMES and CMVN strains, was positioned between two AFLP markers, E33/M48-132 and E40/M47-262, on pepper chromosome 12 and explained 45.0-63.6% of the phenotypic variation (Caranta et al. 2002). CMV resistance in C. annuum ‘BJ0747-1-3-1-1’ was controlled by six QTLs, qcmv.hb-4.1, -7.1, -8.1, -8.2, -8.3, and -16.1, derived from experiments conducted over two growing seasons (summer and autumn) (Yao et al. 2013). Two stable and major QTLs, qcmv.hb-8.2 and -4.1, were found on linkage groups 8 and 4, and explained 37.7-43.5% and 10.7-11.2% of the trait variation, respectively (Yao et al. 2013). In the same population, three QTLs, qcmv11.1, qcmv11.2, and qcmv12.1, conferring CMV resistance were additionally detected using SLAF-seq with trait variation of 10.2%, 19.2%, and 7.3%, respectively (Li et al. 2018). Recently, two QTLs, qCmr2.1 and qCmr11.1, were identified through genome-wide comparison of SNP profiles between the CMV-resistant and CMV-susceptible bulks constructed from an F2 population of C. frutescens ‘PBC688’ (resistant) and C. annuum ‘G29’ (susceptible), and the gene CA02g19570 was identified as a possible candidate gene of qCmr2.1 (Guo et al. 2017a).
Only in C. annuum ‘Bukang’, the CMV resistance was controlled by single dominant gene Cmr1 (Kang et al. 2010). Three CMVKorean and CMVFNY resistance SNP markers, CaTm-int3HRM, CaT1616BAC, and 240H02sp6 associated with Cmr1 gene, were developed through the comparative genetic mapping between pepper and tomato (Kang et al. 2010). Besides, a total of 1,941 Capsicum accessions were evaluated using the 240H02sp6 marker, of which 89 and 162 were homozygously and heterozygously resistant, respectively (Ro et al. 2012).
In Korea, CMVP1 strain breaking the CMVP0 resistance of pepper in the field was first reported in 2006 (Lee et al. 2006). A total of 10 CMVP1-resistant peppers were identified by evaluating 199 pepper genetic resources using enzyme-linked immunosorbent assays (ELISA) (Shin et al. 2013). The CMVP1 resistance of C. annuum ‘I7339’ was controlled by two different recessive genes, cmr3E and cmr3L, which were linked with one RAPD marker OPAT16 on pepper chromosome 6 (Min et al. 2014). Recently, two QTLs cmvP1-5.1 and cmvP1-10.1, conferring CMVP1 resistance were identified with trait variation of 17.81% and 22.78%, respectively (Eun et al. 2016). Furthermore, a single recessive gene, cmr2, conferring a broad-spectrum type of resistance to CMVP1 in C. annuum ‘Lam32’ was identified by inheritance analysis, and a SNP marker, Affy4, positioned 2.3 cM from the gene on chromosome 8 (Choi et al. 2018).

Tobamoviruses

Capsicum plants have genes, designated L genes, conferring resistance to Tobamovirus spp. which generate diverse symptoms including the chlorosis of leaves, stunting, and distorted and lumpy fruiting structures (Boukema 1980). There are four resistant alleles for L locus: L1 (derived from C. annuum accessions) confers resistance to P0 pathotype viruses such as Tomato mosaic virus (ToMV); L2 (C. frutescens) confers resistance to P0 and P1 pathotype Paprika mild mottle virus (PaMMV) that overcomes L1 resistance; L3 (C. chinense) confers resistance to P0, P1, and P1,2 pathotype Pepper mild mottle virus (PMMoV) that overcomes L2 resistance; L4 (C. chacoense) confers resistance to P0, P1, P1,2, and P1,2,3 pathotype PMMoV that overcomes L3 resistance (Boukema 1980, 1982, 1984; Tsuda et al. 1998; Tomita et al. 2008, 2011). The genes conferring resistance to various tobamoviruses and their markers were listed in Table 3.
A RAPD marker WA31-1500, linked to the L4 allele that confers resistance to PMMoV, was identified using an F2 population derived from a cross between ‘AP-PM04’ (resistant; derived from ‘PI260429’) and ‘Mie-midori’ (susceptible) (Matsunaga et al. 2003). Three SCAR markers; PMFR11269, PMFR11283 and PMFR21200, positioned at a distance of 4.0 cM from the L3 locus, were developed from two RAPD markers, E18272 and E18286, which were developed by applying the BSA method to two DH populations, K9-DH and K9/AC-DH, derived from F1 hybrid ‘K9’ that harbors the L3 gene derived from ‘PI159236’ (Sugita et al. 2004). A SCAR marker L4SC340, which was mapped 1.8 cM from the L4 locus, was developed from an AFLP marker L4-c, which was identified by applying BSA-AFLP method to a near-isogenic BC4F2 population generated by using C. chacoense ‘PI 260429’ (carrying the L4 allele) as a resistant parent (Kim et al. 2008a). A SNP marker 087H03T7 with a distance of 1.5 cM from the L4 locus was developed by sequencing a BAC clone 082F03 that harbors the tomato I2 and potato R3 homologs (Yang et al. 2009).
To clone the L3 gene, fine mapping and BAC library analysis were performed (Tomita et al. 2008). The L3 gene was mapped between I2 homolog marker IH1-04 and BAC-end marker 189D23M by using an intraspecific F2 population (2,016 individuals) of C. annuum (introduced from C. chinense ‘PI152225’) and an interspecific F2 population (3,391 individuals) between C. chinense ‘PI159236’ (L3/L3) and C. frutescence ‘LS1839-2-4’ (L2/L2) (Tomita et al. 2008).
The L4segF&R marker was developed based on the LRR region of the L4 candidate gene identified in previous study and applied to two L4-segregating F2 populations derived from commercial cultivars ‘Special’ and ‘Myoung-sung’ (Yang et al. 2012). The L4segF&R marker, however, did not completely cosegregate with the L4 gene, suggesting that the candidate is not an actual L4 gene (Yang et al. 2012). An L4-specific HRM marker L4RP-3F/L4-RP3R precisely detected the L4 allele in 90 out of 91 lines (Yang et al. 2012). Furthermore, a set of allele-specific markers of L locus, including L1-SCAR, L2-CAPS, L3-SCAR, L4-SCAR, L0c-SCAR, and L0nu-CAPS markers, was developed using five pepper differential hosts including C. annuum ‘ECW’ (L0/L0), C. annuum ‘Tisana’ (L1/L1), C. annuum ‘CM334’ (L2/L2), C. chinense ‘PI159236’ (L3/L3), and C. chacoense ‘PI260429’ (L4/L4) (Lee et al. 2012a).

Potyviruses

The genus Potyvirus contains over 180 distinct viruses including Potato virus Y (PVY), Tobacco etch virus (TEV), and Pepper mottle virus (PepMoV), most of which cause significant losses in many agriculturally important Solanaceous crops such as tomato, pepper, potato, and tobacco (Caranta et al. 1997a; Kyle and Palloix 1997). Capsicum species have various potyvirus resistance genes such as; pvr1 (C. chinense ‘PI159236’ and ‘PI152225’), pvr21 (C. annuum ‘Yolo RP10’ and ‘Yolo Y’), pvr22 (C. annuum ‘PI264281’, ‘SC46252’, and ‘Florida VR2’), pvr3 (C. annuum ‘Avelar’), Pvr4 (C. annuum ‘CM334’ and ‘Serrano Criollo de Morelos’), pvr5 (C. annuum ‘CM334’ and ‘Serrano Criollo de Morelos’), pvr6 (C. annuum ‘Perennial’), and Pvr7 (C. chinense ‘PI159236’) (Caranta et al. 1996; Kyle and Palloix 1997; Grube et al. 2000a). These genes were mapped with molecular markers and cloned by map-based cloning or candidate gene approach (Tables 3 and 5).
A recessive resistance pvr1 gene against PepMoV and TEV was mapped to a small linkage group, containing TG56, A313, TG135, and CT128b markers, with synteny to the short arm of tomato chromosome 3 (Murphy et al. 1998). The pvr1 gene encodes a translation initiation factor eIF4E and is allelic with pvr21 and pvr22, previously known to be eIF4E with narrower resistance spectra (Kang et al. 2005). Two additional resistant alleles, pvr11 and pvr12, were identified (Kang et al. 2005), and three CAPS markers, Pvr1-S, pvr1-R1, and pvr1-R2, were developed to discriminate between Pvr1+, pvr1, pvr11, and pvr12 alleles (Yeam et al. 2005). Four functional markers, eIF4E-T200A, eIF4E-T236G, eIF4E-G325A, and eIF4E-A614G, were designed for distinguishing between pvr2+, pvr21, pvr22, and pvr23 alleles using the tetra-primer amplification refractory mutation system (ARMS)-PCR method (Rubio et al. 2008). Polymorphism analysis of the pvr2-eIF4E coding sequence in 25 C. annuum accessions revealed 10 allelic variants; pvr21, pvr22, pvr23, pvr24, pvr25, pver26, pver27, pver28, pvr29, and pvr1 (Charron et al. 2008). User-friendly markers for the pvr1 gene were also developed using the Kompetitive Allele-Specific PCR (KASP) genotyping system (Holdsworth and Mazourek 2015).
A recessive pvr3 gene for PepMoV resistance from C. annuum ‘Avelar’ was reported to be different from the pvr1 gene for PepMoV and TEV resistance from C. chinense ‘PI159236’ and ‘PI152225’ (Murphy et al. 1998).
A dominant Pvr4 gene for PVY and PepMoV resistance from C. annuum ‘CM334’ was located on pepper chromosome 10 (Dogimont et al. 1996; Grube et al. 2000a). The Pvr4 gene was mapped on a linkage group containing eight AFLP markers; E33/M54-126, E41/M49-645, E38/M61-403, -414, -460, E41/M55-102, E41/M49-296, and E41/M54-138, and one of them, E41/M49-645 was converted into a CAPS marker (Caranta et al. 1999). RAPD and SCAR markers, UBC191432 and SCUBC191432, linked to the Pvr4 locus were developed using segregating progenies obtained by crossing a homozygous resistant variety (‘Serrano Criollo de Morelos-334’) with a homozygous susceptible variety (‘Yolo Wonder’) (Arnedo-Andrés et al. 2002). Interestingly, trichome density of pepper main stem was tightly linked to the Pvr4 gene resistant to PepMoV (Kim et al. 2011). A cosegregating marker, MY1421, with Pvr4 gene was identified using an NGS method for which a total of 204 F2 individuals derived from a cross between C. annuum ‘SR-231’ (susceptible) and ‘CM334’ (resistant) were used (Devran et al. 2015).
The complementation between recessive pvr6 (‘Perennial’) and pvr22 (‘Florida VR2’) genes confers complete resistance to PVMV (Caranta et al. 1996). The pvr6 gene was positioned on linkage group 4 (LG4) of a pepper map generated by using a DH population from the hybrid between ‘Perennial’ and ‘Yolo Wonder’ (Caranta et al. 1997a). The pvr6 gene was identified to correspond to an eIF(iso)4E gene which encodes the second cap-binding isoform identified in plants (Ruffel et al. 2006). Two simultaneous recessive alleles at pvr2 (eIF4E) and pvr6 (eIFiso4E) loci confer resistance to PVMV as well as Chili veinal mottle virus (ChiVMV) in pepper (Ruffel et al. 2006; Hwang et al. 2009).
A dominant Pvr7 gene confers resistance to the PepMoV Florida (V1182) strain and is tightly linked to the Pvr4 gene with a genetic distance of 0.012 to 0.016 cM and to Tsw gene on pepper chromosome 10 (Grube et al. 2000a). Recently, Pvr7 (C. chinense ‘PI159236’ and C. annuum ‘9093’) and Pvr4 (C. annuum ‘CM334’) were revealed to be the same dominant resistant gene through sequence analysis of the Pvr7 flanking markers and the Pvr4-specific gene (Venkatesh et al. 2018).
The resistance of Pvr9 gene, which is an ortholog of Rpi-blb2 conferring a hypersensitive response (HR) to PepMoV in Nicotiana benthamiana, was characterized in a transient expression system in N. benthamiana (Tran et al. 2015).
In addition, a dominant Cvr1 (C. annuum ‘CV3’) and a recessive cvr4 (C. annuum ‘CV9’) genes were reported to confer ChiVMV resistance (Lee et al. 2017). Recently, a new resistance gene to Pepper yellow mosaic virus (PepYMV), that is different from Pvr4 was reported in C. annuum ‘PIM-025’ (Rezende et al. 2019).

Tomato spotted wilt virus

Tomato spotted wilt virus (TSWV) disease is identified by various symptoms including ringspots (yellow or brown rings) or other line patterns, black streaks on petioles or stems, necrotic leaf spots, or tip dieback (Boiteux et al. 1993). The resistance was found to be determined by a single dominant gene, Tsw, in three C. chinense accessions (‘PI152225’, ‘PI159236’, and ‘7204’) (Moury et al. 1997). There are a few reports on the development of DNA markers for TSWV resistance in Capsicum spp. (Table 3).
A CAPS marker SCAC568 was developed from the OPAC10593 RAPD marker linked to Tsw gene to assist selection of TSWV resistance in pepper (Moury et al. 2000), and it was applied to paprika cultivars, suggesting that SCAC568 can be deployed in pepper breeding programs in combination with TSWV-resistant cultivars from ‘Zeraim’ (Kim et al. 2008c). The Tsw gene was mapped on pepper chromosome 10 and a RAPD marker Q-06270 was identified using the segregating BC4F1 plants developed by backcrossing C. chinense ‘PI152225’ with C. annuum ‘Cuby’ and ‘Spartacus’ (Jahn et al. 2000). Recently, a genome-based approach cloning revealed that Tsw (CcNBARC575) gene encodes typical NLR proteins (Kim et al. 2017c). However, TSWV isolates breaking the Tsw resistance gene were reported (Hobbs et al. 1994; Moury et al. 1997; Jiang et al. 2017). Moreover, Tsw resistance was overcome by some TSWV isolates from paprika at high temperatures (30 ± 2℃) (Chung et al. 2018). Therefore, a research for the identification of novel and stable TSWV-resistant resources will be necessary.

Bacterial spot

Bacterial spot of pepper causes leaf and fruit spots, which lead to defoliation, sun-scalded fruit, and yield loss (Scherer, https://content.ces.ncsu.edu/bacterial-spot-of-pepper-and-tomato). It is caused by Xanthomonas campestris pv. vesicatoria, which includes race 0 to 10 (Stall et al. 2009). Capsicum species are known to have five dominant and two recessive genes resistant to bacterial spot including Bs1 (C. annuum ‘PI163192’), Bs2 (C. chacoense ‘PI260435’), Bs3 (C. annuum ‘PI271322’), Bs4 (C. pubescens ‘PI235047’), BsT (C. annuum commercial cultivars), bs5 (C. annuum ‘PI163192’ and ‘PI271322’), and bs6 (C. annuum ‘PI163192’ and ‘PI271322’) (Hibberd et al. 1987; Stall et al. 2009). Pepper resistance genes differentially interacts with races of xanthomonads: Bs1 gene confers resistance to races 0, 2, and 5; Bs2 gene confers resistance to races 0, 1, 2, 3, 7, and 8; Bs3 gene confers resistance to races 0, 1, 4, 7, and 9; Bs4 gene confers resistance to races 0, 1, 3, 4, and 6 (Stall et al. 2009). The DNA markers linked to the Bs2, Bs3, and bs5 genes have been reported (Table 4).
The Bs2 resistance gene of pepper was positioned on a high-resolution genetic map constructed by RAPD and AFLP markers and was found to cosegregate with one AFLP marker A2 (Tai et al. 1999a). Three yeast artificial chromosome (YAC) clones, YCA22D8, YCA80H11, and YCA164C12, containing the Bs2 gene, were selected using two probes from the A2 and B3 markers previously developed (Tai and Staskawicz 2000). The Bs2 gene, which encodes a tripartite NBS and an LRR motif, was identified by coexpression with avrBs2 in an Agrobacterium-mediated transient assay (Tai et al. 1999b). Two tetra-primer ARMS-PCR markers, 25-1 and 25-2, were developed for marker-assisted selection of the Bs2 gene in pepper (Truong et al. 2011).
The Bs3 gene governing recognition of the Xanthomonas campestris pv. vesicatoria AvrBs3 protein was mapped using AFLP markers and was delimited within two flanking markers, P23-70 and P22-3, with a genetic distance of 0.13 cM (Pierre et al. 2000). The Bs3 gene was physically delimited within two BAC clones, BAC128 and BAC104, and was located between two markers, B104SP6 and B103T7 (Jordan et al. 2006). Bs3 gene encodes flavin monooxygenases with a previously unknown structure (Römer et al. 2007). The report indicated that recognition specificity between Bs3 and AvrBs3 resides in Bs3 (recognized by AvrBs3) and bs3 (not recognized by AvrBs3 due to a 13-bp insertion) promoters. A codominant SCAR marker PR-Bs3 was developed by designing primers to amplify the indel region of Bs3 and bs3 promoters (Römer et al. 2010). Furthermore, user-friendly markers for the Bs3 gene were developed using the KASP genotyping system (Holdsworth and Mazourek 2015).
Two recessive genes, bs5 and bs6, resistant to a pepper xcv race 6 strain, were identified by using an F2 and two BC populations derived from a cross between ECW12346 (resistant) and ECW123 (susceptible) (Jones et al. 2002). According to Vallejos et al. (2010), these two recessive genes when combined confer full resistance to race 6 and five AFLP markers (PepA2, PepC2, PepF4, PepB7, and PepG4) were linked to the bs5 gene.

Bacterial wilt

Bacterial wilt, caused by a soil-borne pathogen Ralstonia solanacearum, is a serious disease in a wide range of crops including pepper and tomato (Peeters et al. 2013). Five Capsicum accessions, including ‘MC-4’, ‘PBC631’, ‘PBC066’, ‘PBC1347’, and ‘PBC473’, were selected for pepper breeding with bacterial wilt resistance (Lopes and Boiteux 2004). A Malaysian pepper accession ‘LS2341’ (C. annuum) was identified to be highly resistant to R. solanacearum strains from Japan (Mimura and Yoshikawa 2009). In addition, six inbred lines (‘KC350-3-4-2’, ‘KC351-2-2-2-4’, ‘KC980-3-1’, ‘KC995-2-1’, ‘KC999-3-1’, and ‘KC1009-3-2’) resistant to bacterial wilt were reported (Tran and Kim 2010). Inheritance analysis and marker development for the resistance to bacterial wilt were poorly studied (Table 4).
A major QTL Bw1 for bacterial wilt resistance, explaining 33% of genetic variance, was detected on pepper chromosome 1 using a DH population derived from a cross between ‘California Wonder’ (susceptible) and ‘LS2341’ (resistant) and an SSR marker CAMS451 was identified to be closely linked to Bw1 (Mimura et al. 2009). A total of six polymorphic AFLP bands, three bands (103, 117, and 161 bp) linked with the resistant recessive allele and three bands (183, 296, and 319 bp) linked with the dominant susceptible allele of the bacterial wilt resistance gene, were detected using C. annuum ‘Pusa Jwala’ (highly susceptible), ‘Ujwala’ (highly resistant), and ‘Anugraha’ (a resistant near isogenic line to ‘Pusa Jwala’) through a BSA-AFLP approach (Thakur et al. 2014). Recently, a major QTL, qRRs-10.1, conferring bacterial wilt resistance was identified in an F2 population of BVRC25 (susceptible) × BVRC1 (resistant) using SLAF-BSA analysis, and the SNP marker ID10-194305124 tightly linked to the QTL peak was developed (Du et al. 2019).

Root-knot nematode

The root-knot nematode (Meloidogyne spp.), which often shows symptoms of stunting, wilting or chlorosis (yellowing), is a major plant pathogen, diseasing several solanaceous crops including pepper (Djian-Caporalino et al. 2007). At least 10 dominant Me genes (N, Me1, Me2, Me3, Me4, Me5, Me6, Me7, Mech1, and Mech2) were reported to be resistant to the nematode (Djian-Caporalino et al. 1999, 2001, 2007). Accordingly, Me4, Me5, Mech1, and Mech2 are specific to certain Meloidogyne species or populations and N, Me1, Me3, and Me7 are effective against a wide range of Meloidogyne species including M. arenaria, M. javanica, and M. incognita. In C. annuum accessions, ‘PI201234’ has Me1 and Mech2 genes, ‘PI322719’ has Me3 and Me4 genes, and ‘CM334’ has Me7 and Mech1 genes (Djian-Caporalino et al. 2007). These genes are clustered on pepper chromosome 9 (Fig. 1, Table 4).
The Me3 and Me4 genes conferring heat-stable resistance to root-knot nematodes were mapped using DH lines and F2 progeny from a cross between ‘Yolo Wonder’ (susceptible) and ‘PM687’ (resistant) by using RAPD and AFLP analyses combined with BSA (Djian-Caporalino et al. 2001). A RAPD marker Q04_0.3 (10.1 cM) and an RFLP marker CT135 (2.7 cM) were linked to the Me3 gene, which was positioned at 10 cM of genetic distance from Me4 gene (Djian-Caporalino et al. 2001). The six-dominant root-knot nematode resistance genes (Me1, Me3, Me4, Me7, Mech1, and Mech2) were found to be clustered in a single genomic region within 28 cM on the pepper chromosome 9 (Djian-Caporalino et al. 2007). Another root-knot nematode resistance gene, N-gene, was co-localized in the Me-genes cluster on pepper chromosome 9 (Fazari et al. 2012). A codominant CAPS marker, CL000081-0555, located 1.13 cM away from the Me1 gene, was developed using an F2 population of a cross between C. annuum ‘AZN-1’ (susceptible line) and ‘PM217’ (resistant inbred line derived from ‘PI201234’) (Uncu et al. 2015). An SSR marker (0.8 cM away) tightly linked to the N gene was developed through fine mapping of NBS-coding resistance genes to the Me-gene cluster on pepper chromosome 9 (Celik et al. 2016). The SCAR_PM54 marker was identified to be fully consistent with artificial nematode (M. incognita race 2) testing, correctly predicting resistant (‘PM687’, ‘PM217’, and ‘Carolina Cayenne’) and susceptible (‘Yolo Wonder B’, ‘California Wonder 300’, and ‘CM331’) genotypes (Pinar et al. 2016). Two BAC clones, PE25F15 and PE11F6, containing the Me3 gene, were identified using BAC library and physical mapping analysis (Guo et al. 2017b). Recently, two markers, an HRM marker 16830-H-V2 and a CAPS marker 16830-CAPS, tightly linked to the Me1 gene, were developed through a fine mapping approach and the CA09g16830 gene was identified as a candidate gene for Me1 (Wang et al. 2018). In addition, a recent development was the identification of nine SNP markers cosegregating with RKN resistance gene (Me7) for the utilization in MAS and the characterization of 25 NLR class candidate resistance genes spanning the Me7 region (Changkwian et al. 2019).

GENE CLONING FOR PEPPER DISEASE RESISTANCE

To date, many disease resistance (R) genes have been identified and characterized in diverse plants (Dangl and Jones 2001; Gururani et al. 2012; Kourelis and van der Hoom 2018). The plant R genes can specifically detect a pathogen attack and promote a counter-attack system against the pathogen (van der Biezen and Jones 1998; Shehzadi et al. 2017). These R genes encode NLR and non-NLR type proteins, which play important roles in effector-triggered immunity (ETI) plant defense (Jacob et al. 2013). In pepper, a total of 755 NLR-encoding genes, including 27 TNL, 236 CNL, 159 NL, 15 TN, 143 CN, and 175 N type genes, were identified through genome-wide analysis (Seo et al. 2016). In addition, 25 Pto-like protein kinases (PLPKs), which were non-NLR type proteins, were identified in pepper genome (Venkatesh et al. 2016).
In light of the rapidly evolving molecular markers and map-based cloning, identification and characterization of disease resistance genes in Capsicum species have advanced the pace of introgression of resistance genes into elite varieties (Srivastava and Mangal 2019). Fine mapping and identification of resistance genes and QTLs have prompted the discovery of several resistance genes in pepper (Table 5). The Bs2 gene, which encodes an NLR protein that interacts with the corresponding bacterial avirulence protein avrBs2, conferring resistance to Xanthomonas campestris pv. vesicatoria (Xcv) was the first cloned disease resistance gene in pepper (Tai et al. 1999b). Two recessive genes, pvr1 and pvr6, which encode eIF4E and eIF(iso)4E proteins, respectively, were cloned and reported to confer resistance to potyviruses such as PepMoV, PVMV, and ChiVMV (Kang et al. 2005; Ruffel et al. 2006). The Bs3 gene resistant to the Xcv with AvrBs3 was identified to encode flavin monooxygenase, which is an unusual protein encoded by plant disease resistance genes (Römer et al. 2007). According to the report, AvrBs3 protein interacts with the promoter region of Bs3 gene for the activation of the gene. L3 gene, a typical NLR protein encoding gene, conferring resistance to P0, P1, and P1,2 pathotypes of Tobamovirus, was revealed by map-based cloning, while other alleles of the L locus, including L1, L1a, L1c, L2, L2b, and L4, were identified by a homology-based search (Tomita et al. 2011). The major QTL Pc5.1 for resistance to P. capsici in C. annuum ‘CM334’ cosegregates with the CaDMR1 gene encoding a homoserine kinase (Rehrig et al. 2014). The other major QTL CaPhyto, conferring resistance to P. capsici Leonian race 2 in C. annuum ‘PI201234’, has two candidate genes, Capana05g000764 and Capana05g000769 (Wang et al. 2016). Map-based cloning detected two resistance genes, Pvr4 (a potyvirus resistance gene) and Tsw (a TSWV resistance gene), encoding the NLR proteins at the same locus on chromosome 10 in two different Capsicum species (Kim et al. 2017c). The gene CA02g19570 was identified as a candidate gene of the major QTL qCmr2.1 controlling CMV resistance using a SLAF-seq method (Guo et al. 2017a). Gene prediction of a single dominant resistance gene PMR1 revealed two putative genes (408 and 556) of the NLR resistance gene family which belongs to the loci responsible for the resistance of powdery mildew (Jo et al. 2017). Fine mapping of the Me1 gene conferring a heat-stable and broad-spectrum resistance to root-knot nematodes revealed the CA09g16830 gene, which is a homolog of R1A-3 gene encoding a putative late blight resistance protein (Wang et al. 2018).

FUTURE PROSPECTS

Despite the increasing demand for chili pepper, diverse pepper diseases are the primary limiting factors of yield and quality of its fruits worldwide. Moreover, the emerging and re-emerging of pathogens and the likelihood of resistance breakdown has posed a heavy burden to the chili pepper breeders. In the last two decades, the application of molecular markers, specifically the genetic mapping of disease resistance genes has seen a boom in the detection of QTLs associated with resistance to the most pressing diseases of chili pepper. The number of cloned resistance genes in Capsicum species is increasing amid the advances in molecular cloning (Table 5), and these genes are widely and unevenly dispersed in C. annuum genome (Fig. 1). Therefore, the targeted multi-loci genotyping system, including Fluidigm nanofluidic dynamic arrays (Wang et al. 2009; Kim et al. 2017a), targeted amplicon sequencing (TAS) (Bybee et al. 2011; Clarke et al. 2014), and genome-tagged amplification (GTA) (Ho et al. 2014), is so imperative to develop pepper varieties with multiple disease resistance by pyramiding of diverse disease resistance genes. Although the techniques for genome-wide SNP discovery, genetic linkage mapping, and candidate gene identification through NGS analysis have made much progress in Capsicum disease-resistance breeding research, genetic transformation (Altpeter et al. 2016) and genome editing (Yin et al. 2017; Langner et al. 2018) technologies for pepper still remains unsolved, hence are ways forward (van Eck 2018). Many researches employing these techniques will be necessary for the functional analysis of candidate genes, breeding and the rapid development of new disease resistant pepper varieties.

CONCLUSION

In this review, the development of DNA markers closely linked to genes conferring resistance to ten major diseases of C. annuum and cloned genes were summarized. QTL mapping of resistance genes and their inheritance analysis showed diverse types of resistance genes encompassing single, multiple and cluster of resistance gene(s). The development of an enormous number of DNA markers linked to resistance genes and map-based cloning of resistance genes could substantially advance the genetic improvement of chili pepper for diverse disease resistance. The development of pepper varieties with multiple disease resistance would significantly limit the frequency of resistance breakdown and thereby mitigate the yield and quality loss caused by the infection of pathogens.

ACKNOWLEDGEMENTS

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean Government (Ministry of Science and ICT, MSIT, grant No. NRF-2018R1C1B6002688).

REFERENCES

Altpeter F., Springer NM., Bartley LE., Blechl AE., Brutnell TP., Citovsky V, et al. 2016. Advancing crop transformation in the era of genome editing. Plant Cell. 28:1510–1520. DOI: 10.1105/tpc.16.00196. PMID: 27335450. PMCID: PMC4981132.
[CrossRef] [Google Scholar]
Arnedo-Andrés MS., Gil-Ortega R., Luis-Arteaga M., Hormaza JI. 2002. Development of RAPD and SCAR markers linked to the Pvr4 locus for resistance to PVY in pepper (Capsicum annuum L.). Theor. Appl. Genet. 105:1067–1074. DOI: 10.1007/s00122-002-1058-2. PMID: 12582935.
[CrossRef] [PDF] [Google Scholar]
AVRDC. 2003. Host resistance to pepper anthracnose. Progress Report 2002. AVRDC - the World Vegetable Center;Shanhua, Taiwan:
[Google Scholar]
Barchenger DW., Naresh P., Kumar S. Ramchiary N., Kole C., editors2019. Genetic resources of Capsicum. The Capsicum Genome, Compendium of Plant Genomes. Springer Nature Switzerland AG;Switzerland: p. 9–23. DOI: 10.1007/978-3-319-97217-6_2.
[CrossRef] [Google Scholar]
Ben Chaim., Grube RC., Lapidot M., Jahn M., Paran I. 2001. Identification of quantitative trait loci associated with resistance to cucumber mosaic virus in Capsicum annuum. Theor. Appl. Genet. 102:1213–1220. DOI: 10.1007/s001220100581.
[CrossRef] [PDF] [Google Scholar]
Boiteux LS., Nagata T., Dutra WP., Fonseca MEN. 1993. Source of resistance to tomato spotted wilt virus (TSWV) in cultivated and wild species of Capsicum. Euphytica. 67:89–94. DOI: 10.1007/BF00022729.
[CrossRef] [PDF] [Google Scholar]
Boukema IW. 1980. Allelism of genes controlling resistance to TMV in Capsicum L. Euphytica. 29:433–439. DOI: 10.1007/BF00025143.
[CrossRef] [PDF] [Google Scholar]
Boukema IW. 1982. Resistance to a new strain of TMV in Capsicum chacoense Hunz. Capsicum Newsletter. 1:49–51.
[Google Scholar]
Boukema IW. 1984. Resistance to TMV in Capsicum chacoense Hunz. Is governed by allele of the L-locus. Capsicum Newsletter. 3:47–48.
[Google Scholar]
Bybee SM., Bracken-Grissom H., Haynes BD., Hermansen RA., Byers RL., Clement MJ, et al. 2011. Targeted amplicon sequencing (TAS): A scalable next-gen approach to multilocus, multitaxa phylogenetics. Genome Biol. Evol. 3:1312–1323. DOI: 10.1093/gbe/evr106. PMID: 22002916. PMCID: PMC3236605.
[CrossRef] [PDF] [Google Scholar]
Caranta C., Lefebvre V., Palloix A. 1997a. Polygenic resistance of pepper to potyviruses consists of a combination of isolate-specific and broad-spectrum quantitative trait loci. Mol. Plant Microbe Interact. 10:872–878. DOI: 10.1094/MPMI.1997.10.7.872.
[CrossRef] [Google Scholar]
Caranta C., Palloix A., Gebre-Selassie K., Lefebvre V., Moury B., Daubèze AM. 1996. A complementation of two genes originating from susceptible Capsicum annuum lines confers a new and complete resistance to pepper veinal mottle virus. Phytopathology. 86:739–743. DOI: 10.1094/Phyto-86-739.
[CrossRef] [Google Scholar]
Caranta C., Palloix A., Lefebvre V., Daubèze AM. 1997b. QTLs for a component of partial resistance to cucumber mosaic virus in pepper: restriction of virus installation in host-cells. Theor. Appl. Genet. 94:431–438. DOI: 10.1007/s001220050433.
[CrossRef] [PDF] [Google Scholar]
Caranta C., Pflieger S., Lefebvre ., Daubèze AM., Thabuis A., Palloix A. 2002. QTLs involved in the restriction of cucumber mosaic virus (CMV) long-distance movement in pepper. Theor. Appl. Genet. 104:586–591. DOI: 10.1007/s001220100753. PMID: 12582662.
[CrossRef] [PDF] [Google Scholar]
Caranta C., Thabuis A., Palloix A. 1999. Development of a CAPS marker for the Pvr4 locus: A tool for pyramiding potyvirus resistance genes in pepper. Genome. 42:1111–1116. DOI: 10.1139/gen-42-6-1111. PMID: 10659777.
[CrossRef] [Google Scholar]
Celik I., Sogut MA., Ozkaynak E., Doganlar S., Frary A. 2016. Physical mapping of NBS-coding resistance genes to the Me-gene cluster on chromosome P9 reveals markers tightly linked to the N gene for root-knot nematode resistance in pepper. Mol. Breed. 36:137. DOI: 10.1007/s11032-016-0560-1.
[CrossRef] [Google Scholar]
Changkwian A., Venkatesh J., Lee JH., Han JW., Kwon JK., Siddique MI, et al. 2019. Physical localization of the root-knot nematode (Meloidogyne incognita) resistance locus Me7 in pepper (Capsicum annuum). Front. Plant Sci. 10:886. DOI: 10.3389/fpls.2019.00886. PMID: 31354762. PMCID: PMC6629957.
[CrossRef] [Google Scholar]
Charron C., Nicolai M., Gallois JL., Robaglia C., Moury B., Palloix A, et al. 2008. Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyvirus VPg. Plant J. 54:56–68. DOI: 10.1111/j.1365-313X.2008.03407.x. PMID: 18182024.
[CrossRef] [Google Scholar]
Choi S., Lee JH., Kang WH., Kim J., Huy HN., Park SW, et al. 2018. Identification of cucumber mosaic resistance 2 (cmr2) that confers resistance to a new cucumber mosaic virus isolate P1 (CMV-P1) in pepper (Capsicum spp.). Front. Plant Sci. 9:1106. DOI: 10.3389/fpls.2018.01106. PMID: 30186289. PMCID: PMC6110927.
[CrossRef] [Google Scholar]
Chung BN., Lee JH., Kang BC., Koh SW., Joa JH., Choi KS, et al. 2018. HR-mediated defense response is overcome at high temperatures in Capsicum species. Plant Pathol. J. 34:71–77. DOI: 10.5423/PPJ.NT.06.2017.0120. PMID: 29422790. PMCID: PMC5796752.
[CrossRef] [Google Scholar]
Clarke LJ., Czechowski P., Soubrier J., Stevens MI., Cooper A. 2014. Modular tagging of amplicons using a single PCR for high-throughput sequencing. Mol. Ecol. Resour. 14:117–121. DOI: 10.1111/1755-0998.12162. PMID: 24028345.
[CrossRef] [Google Scholar]
Cobb JN., Biswas PS., Platten JD. 2019. Back to the future: revisiting MAS as a tool for modern plant breeding. Theor. Appl. Genet. 132:647–667. DOI: 10.1007/s00122-018-3266-4. PMID: 30560465. PMCID: PMC6439155.
[CrossRef] [PDF] [Google Scholar]
Dangl JL., Jones JDG. 2001. Plant pathogens and integrated defence responses to infection. Nature. 411:826–833. DOI: 10.1038/35081161. PMID: 11459065.
[CrossRef] [PDF] [Google Scholar]
Daubeze AM., Hennart JW., Palloix A. 1995. Resistance to Leveillula taurica in pepper (Capsicum annuum) is oligogenically controlled and stable in Mediterranean regions. Plant Breed. 114:327–332. DOI: 10.1111/j.1439-0523.1995.tb01243.x.
[CrossRef] [Google Scholar]
de Souza., Café-Filho AC. 2003. Resistance to Leveillula taurica in the genus Capsicum. Plant Pathol. 52:613–619. DOI: 10.1046/j.1365-3059.2003.00920.x.
[CrossRef] [Google Scholar]
Deschamps S., Llaca V., May GD. 2012. Genotyping-by-sequencing in plants. Biology (Basel). 1:460–483. DOI: 10.3390/biology1030460. PMID: 24832503. PMCID: PMC4009820.
[CrossRef] [Google Scholar]
Devran Z., Kahveci E., Özkaynak E., Studholme DJ., Tör M. 2015. Development of molecular markers tightly linked to Pvr4 gene in pepper using next-generation sequencing. Mol. Breed. 35:101. DOI: 10.1007/s11032-015-0294-5. PMID: 25798050. PMCID: PMC4361654.
[CrossRef] [Google Scholar]
Djian-Caporalino C., Fazari A., Arguel MJ., Vernie T., VandeCasteele C., Faure I, et al. 2007. Root-knot nematode (Meloidogyne spp.) Me resistance genes in pepper (Capsicum annuum L.) are clustered on the P9 chromosome. Theor. Appl. Genet. 114:473–486. DOI: 10.1007/s00122-006-0447-3. PMID: 17136373.
[CrossRef] [PDF] [Google Scholar]
Djian-Caporalino C., Pijarowski L., Fazari A., Samson M., Gaveau L., O'Byrne C, et al. 2001. High-resolution genetic mapping of the pepper (Capsicum annuum L.) resistance loci Me3 and Me4 conferring heat-stable resistance to root-knot nematodes (Meloidogyne spp.). Theor. Appl. Genet. 103:592–600. DOI: 10.1007/PL00002914.
[CrossRef] [PDF] [Google Scholar]
Djian-Caporalino C., Pijarowski L., Januel A., Lefebvre V., Daubèze A., Palloix A, et al. 1999. Spectrum of resistance to root-knot nematodes and inheritance of heat-stable resistance in pepper (Capsicum annuum L.). Theor. Appl. Genet. 99:496–502. DOI: 10.1007/s001220051262. PMID: 22665183.
[CrossRef] [PDF] [Google Scholar]
Dogimont C., Palloix A., Daubze AM., Marchoux G., Selassie KG., Pochard E. 1996. Genetic analysis of broad spectrum resistance to potyviruses using doubled haploid lines of pepper (Capsicum annuum L.). Euphytica. 88:231–239. DOI: 10.1007/BF00023895.
[CrossRef] [PDF] [Google Scholar]
Du H., Wen C., Zhang X., Xu X., Yang J., Chen B, et al. 2019. Identification of a major QTL (qRRs-10.1) that confers resistance to Ralstonia solanacearum in pepper (Capsicum annuum) using SLAF-BSA and QTL mapping. Int. J. Mol. Sci. 20:5887. DOI: 10.3390/ijms20235887. PMID: 31771239. PMCID: PMC6928630.
[CrossRef] [Google Scholar]
Eun MH., Han JH., Yoon JB., Lee J. 2016. QTL mapping of resistance to the Cucumber mosaic virus P1 strain in pepper using a genotyping-by-sequencing analysis. Hortic. Environ. Biote. 57:589–597. DOI: 10.1007/s13580-016-0128-3.
[CrossRef] [PDF] [Google Scholar]
Fazari A., Palloix A., Wang LH., Hua MY., Sage-Palloix AM., Zhang BX, et al. 2012. The root-knot nematode resistance N-gene co-localizes in the Me-genes cluster on the pepper (Capsicum annuum L.) P9 chromosome. Plant Breed. 131:665–673. DOI: 10.1111/j.1439-0523.2012.01994.x.
[CrossRef] [Google Scholar]
Grube RC., Blauth JR., Arnedo AMS., Caranta C., Jahn MK. 2000a. Identification and comparative mapping of a dominant potyvirus resistance gene cluster in Capsicum. Theor. Appl. Genet. 101:852–859. DOI: 10.1007/s001220051552.
[CrossRef] [PDF] [Google Scholar]
Grube RC., Zhang Y., Murphy JF., Loaiza-Figueroa F., Lackney VK., Provvidenti R, et al. 2000b. New source of resistance to Cucumber mosaic virus in Capsicum frutescens. Plant Dis. 84:885–891. DOI: 10.1094/PDIS.2000.84.8.885. PMID: 30832143.
[CrossRef] [Google Scholar]
Guo G., Wang S., Liu J., Pan B., Diao W., Ge W, et al. 2017a. Rapid identification of QTLs underlying resistance to Cucumber mosaic virus in pepper (Capsicum frutescens). Theor. Appl. Genet. 130:41–52. DOI: 10.1007/s00122-016-2790-3. PMID: 27650192.
[CrossRef] [PDF] [Google Scholar]
Guo X., Yang XH., Yang Y., Mao ZC., Liu F., Ma WQ, et al. 2017b. Bacterial artificial chromosome library construction of root-knot nematode resistant pepper genotype HDA149 and identification of clones linked to Me3 resistant locus. J. Intergr. Agric. 16:57–64. DOI: 10.1016/S2095-3119(16)61446-6.
[CrossRef] [Google Scholar]
Gururani MA., Venkatech J., Upadhyaya CP., Nookaraju A., Pandey SK., Park SW. 2012. Plant disease resistance genes: Current status and future directions. Physiol. Mol. Plant P. 78:51–65. DOI: 10.1016/j.pmpp.2012.01.002.
[CrossRef] [Google Scholar]
Hibberd AM., Bassett MJ., Stall RE. 1987. Allelism tests of three dominant genes for hypersensitive resistance to bacterial spot of pepper. Phytopathology. 77:1304–1307. DOI: 10.1094/Phyto-77-1304.
[CrossRef] [Google Scholar]
Ho T., Cardle L., Xu X., Bayer M., Prince KSJ., Mutava RN, et al. 2014. Genome-Tagged Amplification (GTA): a PCR-based method to prepare sample-tagged amplicons from hundreds of individuals for next generation sequencing. Mol. Breed. 34:977–988. DOI: 10.1007/s11032-014-0090-7.
[CrossRef] [PDF] [Google Scholar]
Hobbs HA., Black LL., Johnson RR., Valverde RA. 1994. Differences in reactions among tomato spotted wilt virus isolates to three resistant Capsicum chinense lines. Plant Dis. 78:1220. DOI: 10.1094/PD-78-1220D.
[CrossRef] [Google Scholar]
Holdsworth WL., Mazourek M. 2015. Development of user-friendly markers for the pvr1 and Bs3 disease resistance genes in pepper. Mol. Breed. 35:28. DOI: 10.1007/s11032-015-0260-2.
[CrossRef] [Google Scholar]
Huq MA., Akter S., Jung YJ., Nou IS., Cho YG., Kang KK. 2016. Genome sequencing, a milstone for genomic research and plant breeding. Plant Breed. Biotech. 4:29–39. DOI: 10.9787/PBB.2016.4.1.29.
[CrossRef] [PDF] [Google Scholar]
Hwang JN., Li J., Liu WY., An SJ., Cho H., Her NH, et al. 2009. Double mutations in eIF4E and eIFiso4E confer recessive resistance to chili veinal mottle virus in pepper. Mol. Cells. 27:329–336. DOI: 10.1007/s10059-009-0042-y. PMID: 19326080.
[CrossRef] [PDF] [Google Scholar]
Jacob F., Vernaldi S., Maekawa T. 2013. Evolution and conservation of plant NLR functions. Front. Immunol. 4:297. DOI: 10.3389/fimmu.2013.00297. PMID: 24093022. PMCID: PMC3782705.
[CrossRef] [Google Scholar]
Jahn M., Paran I., Hoffmann K., Radwanski ER., Livingstone KD., Grube RC, et al. 2000. Genetic mapping of the Tsw locus for resistance to the Tospovirus Tomato spotted wilt virus in Capsicum spp. and its relationship to the Sw-5 gene for resistance to the same pathogen in tomato. Mol. Plant Microbe Interact. 13:673–682. DOI: 10.1094/MPMI.2000.13.6.673. PMID: 10830267.
[CrossRef] [Google Scholar]
Jiang L., Huang Y., Sun L., Wang B., Zhu M., Li J, et al. 2017. Occurrence and diversity of Tomato spotted wilt virus isolates breaking the Tsw resistance gene of Capsicum chinense in Yunnan, southwest China. Plant Pathol. 66:980–989. DOI: 10.1111/ppa.12645.
[CrossRef] [Google Scholar]
Jo J., Venkatesh J., Han K., Lee HY., Choi GJ., Lee HJ, et al. 2017. Molecular mapping of PMR1, a novel locus conferring resistance to powdery mildew in pepper (Capsicum annuum). Front. Plant Sci. 8:2090. DOI: 10.3389/fpls.2017.02090. PMID: 29276524. PMCID: PMC5727091.
[CrossRef] [Google Scholar]
Jones JB., Minsavage GV., Roberts PD., Johnson RR., Kousik CS., Subramanian S, et al. 2002. A non-hypersensitive resistance in pepper to the bacterial spot pathogen is associated with two recessive genes. Phytopathology. 92:273–277. DOI: 10.1094/PHYTO.2002.92.3.273. PMID: 18943998.
[CrossRef] [Google Scholar]
Jordan T., Römer P., Meyer A., Szczesny R., Pierre M., Piffanelli P, et al. 2006. Physical delimitation of the pepper Bs3 resistance gene specifying recognition of the AvrBs3 protein from Xanthomonas campestris pv. vesicatoria. Theor. Appl. Genet. 113:895–905. DOI: 10.1007/s00122-006-0349-4. PMID: 16874489.
[CrossRef] [PDF] [Google Scholar]
Kang BC., Yeam I., Frantz JD., Murphy JF., Jahn MM. 2005. The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J. 42:392–405. DOI: 10.1111/j.1365-313X.2005.02381.x. PMID: 15842624.
[CrossRef] [Google Scholar]
Kang WH., Hoang NH., Yang HB., Kwon JK., Jo SH., Seo JK, et al. 2010. Molecular mapping and characterization of a single dominant gene controlling CMV resistance in peppers (Capsicum annuum L.). Theor. Appl. Genet. 120:1587–1596. DOI: 10.1007/s00122-010-1278-9. PMID: 20180096.
[CrossRef] [PDF] [Google Scholar]
Kim C., Guo H., Kong W., Chandnani R., Shuang LS., Paterson AH. 2016. Application of genotyping by sequencing technology to a variety of crop breeding programs. Plant Sci. 242:14–22. DOI: 10.1016/j.plantsci.2015.04.016. PMID: 26566821.
[CrossRef] [Google Scholar]
Kim H., Yoon JB., Lee J. 2017a. Development of Fluidigm SNP type genotyping assays for marker-assisted breeding of chili pepper (Capsicum annuum L.). Hortic. Sci. Technol. 35:465–479. DOI: 10.12972/kjhst.20170050.
[CrossRef] [Google Scholar]
Kim HJ., Han JH., Kim S., Lee HR., Shin JS., Kim JH, et al. 2011. Trichome density of main stem is tightly linked to PepMoV resistance in chili pepper (Capsicum annuum L.). Theor. Appl. Genet. 122:1051–1058. DOI: 10.1007/s00122-010-1510-7. PMID: 21184049.
[CrossRef] [PDF] [Google Scholar]
Kim HJ., Han JH., Yoo JH., Cho HJ., Kim BD. 2008a. Development of a sequence characteristic amplified region marker linked to the L4 locus conferring broad spectrum resistance to tobamoviruses in pepper plants. Mol. Cells. 25:205–210. PMID: 18414011.
[Google Scholar]
Kim HJ., Nahm SH., Lee HR., Yoon GB., Kim KT., Kang BC, et al. 2008b. BAC-derived markers converted from RFLP linked to Phytophthora capsici resistance in pepper (Capsicum annuum L.). Theor. Appl. Genet. 118:15–27. DOI: 10.1007/s00122-008-0873-5. PMID: 18795251.
[CrossRef] [PDF] [Google Scholar]
Kim HJ., Yang HB., Chung BN., Kang BC. 2008c. Survey and application of DNA markers linked to TSWV resistance. Korean J. Hortic. Sci. Technol. 26:464–470.
[Google Scholar]
Kim S., Kim KT., Kim DH., Yang EY., Cho MC., Jamal A, et al. 2010. Identification of quantitative trait loci associated with anthracnose resistance in chili pepper (Capsicum spp.). Korean J. Hortic. Sci. Technol. 28:1014–1024.
[Google Scholar]
Kim S., Park J., Yeom SI., Kim YM., Seo E., Kim KT, et al. 2017b. New reference genome sequences of hot pepper reveal the massive evolution of plant disease-resistance genes by retroduplication. Genome Biol. 18:210. DOI: 10.1186/s13059-017-1341-9. PMID: 29089032. PMCID: PMC5664825.
[CrossRef] [PDF] [Google Scholar]
Kim S., Park M., Yeom SI., Kim YM., Lee JM., Lee HA, et al. 2014. Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat. Genet. 46:270. DOI: 10.1038/ng.2877. PMID: 24441736.
[CrossRef] [PDF] [Google Scholar]
Kim SB., Kang WH., Huy HN., Yeom SI., An JT., Kim S, et al. 2017c. Divergent evolution of multiple virus-resistance genes from a progenitor in Capsicum spp. New Phytol. 213:886–899. DOI: 10.1111/nph.14177. PMID: 27612097.
[CrossRef] [Google Scholar]
Kim SH., Yoon JB., Do JW., Park HG. 2007. Resistance to anthracnose caused by Colletotrichum acutatum in chili pepper (Capsicum annuum L.). J. Crop Sci. Biotech. 10:277–280.
[Google Scholar]
Kim SH., Yoon JB., Do JW., Park HG. 2008d. A major recessive gene associated with anthracnose resistance to Colletotrichum capsici in chili pepper (Capsicum annuum L.). Breed. Sci. 58:137–141. DOI: 10.1270/jsbbs.58.137.
[CrossRef] [Google Scholar]
Kim SH., Yoon JB., Park HG. 2008e. Inheritance of anthracnose resistance in a new genetic resource, Capsicum baccatum PI594137. J. Crop Sci. Biotech. 11:13–16.
[Google Scholar]
Kourelis J., van der. 2018. Defended to the nines - 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell. 30:285–299. DOI: 10.1105/tpc.17.00579. PMID: 29382771. PMCID: PMC5868693.
[CrossRef] [Google Scholar]
Kumar S., Banks TW., Cloutier S. 2012. SNP discovery through next-generation sequencing and its applications. Int. J. Plant Genomics. 831460. DOI: 10.1155/2012/831460. PMID: 23227038. PMCID: PMC3512287.
[CrossRef] [Google Scholar]
Kyle MM., Palloix A. 1997. Proposed revision of nomenclature for potyvirus resistance genes in Capsicum. Euphytica. 97:183–188. DOI: 10.1023/A:1003009721989.
[CrossRef] [Google Scholar]
Langner T., Kamoun S., Belhaj K. 2018. CRISPR crops: Plant genome editing toward disease resistance. Annu. Rev. Phytopathol. 56:479–512. DOI: 10.1146/annurev-phyto-080417-050158. PMID: 29975607.
[CrossRef] [Google Scholar]
Lapidot M., Paran I., Ben-Joseph R., Ben-Harush S., Pilowsky M., Cohen S, et al. 1997. Tolerance to cucumber mosaic virus in pepper: Development of advanced breeding lines and evaluation of virus level. Plant Dis. 81:185–188. DOI: 10.1094/PDIS.1997.81.2.185. PMID: 30870894.
[CrossRef] [Google Scholar]
Lee J., Do JW., Yoon JB. 2011. Development of STS markers linked to the major QTLs for resistance to the pepper anthracnose caused by Colletotrichum acutatum and C. capsici. Hortic. Environ. Biote. 52:596–601. DOI: 10.1007/s13580-011-0178-5.
[CrossRef] [PDF] [Google Scholar]
Lee J., Han JH., Yoon JB. 2012a. A set of allele-specific markers linked to L locus resistant to Tobamovirus in Capsicum spp. Korean J. Hortic. Sci. Technol. 30:286–293. DOI: 10.7235/hort.2012.12018.
[CrossRef] [PDF] [Google Scholar]
Lee J., Hong JH., Do JW., Yoon JB. 2010. Identification of QTLs for resistance to anthracnose to two Colletotrichum species in pepper. J. Crop Sci. Biotech. 13:227–233. DOI: 10.1007/s12892-010-0081-0.
[CrossRef] [PDF] [Google Scholar]
Lee JH., An JT., Siddique MI., Han K., Choi S., Kwon JK, et al. 2017. Identification and molecular genetic mapping of Chili veinal mottle virus (ChiVMV) resistance genes in pepper (Capsicum annuum). Mol. Breed. 37:121. DOI: 10.1007/s11032-017-0717-6.
[CrossRef] [Google Scholar]
Lee MY., Lee JH., Ahn HI., Yoon JY., Her NH., Choi GS, et al. 2006. Identification and sequence analysis of RNA3 of a resistance breaking Cucumber mosaic virus isolate of Capsicum annuum. Plant Pathol. J. 22:265–270. DOI: 10.5423/PPJ.2006.22.3.265.
[CrossRef] [PDF] [Google Scholar]
Lee WP., Lee J., Han JH., Kang BC., Yoon JB. 2012b. Validity test for molecular markers associated with resistance to Phytophthora root rot in chili pepper (Capsicum annuum L.). Korean J. Hortic. Sci. Technol. 30:64–72. DOI: 10.7235/hort.2012.11112.
[CrossRef] [PDF] [Google Scholar]
Lefebvre V., Daubèze AM., Rouppe van., Peleman J., Bardin M., Palloix A. 2003. QTLs for resistance to powdery mildew in pepper under natural and artificial infections. Theor. Appl. Genet. 107:661–666. DOI: 10.1007/s00122-003-1307-z. PMID: 12819909.
[CrossRef] [PDF] [Google Scholar]
Li N., Yin Y., Wang F., Yao M. 2018. Construction of a high-density genetic map and identification of QTLs for cucumber mosaic virus resistance in pepper (Capsicum annuum L.) using specific length amplified fragment sequencing (SLAF-seq). Breed. Sci. 68:233–241. DOI: 10.1270/jsbbs.17063. PMID: 29875607. PMCID: PMC5982177.
[CrossRef] [Google Scholar]
Liew M., Pryor R., Palais R., Meadows C., Erali M., Lyon E, et al. 2004. Genotyping of single-nucleotide polymorphisms by high-resolution melting of small amplicons. Clin. Chem. 50:1156–1164. DOI: 10.1373/clinchem.2004.032136. PMID: 15229148.
[CrossRef] [PDF] [Google Scholar]
Liu WY., Kang JH., Jeong HS., Choi HJ., Yang HB., Kim KT, et al. 2014. Combined use of bulked segregant analysis and microarrays reveals SNP markers pinpointing a major QTL for resistance to Phytophthora capsici in pepper. Theor. Appl. Genet. 127:2503–2513. DOI: 10.1007/s00122-014-2394-8. PMID: 25208646.
[CrossRef] [PDF] [Google Scholar]
Lopes CA., Boiteux LS. 2004. Biovar-specific and broad-spectrum sources of resistance to bacterial wilt (Ralstonia solanacearum) in Capsicum. Crop Breed. Appl. Biot. 4:350–355. DOI: 10.12702/1984-7033.v04n03a14.
[CrossRef] [Google Scholar]
Mahasuk P., Khumpeng N., Wasee S., Taylor PWJ., Mongkolporn O. 2009a. Inheritance of resistance to anthracnose (Colletotrichum capsici) at seedling and fruiting stages in chili pepper (Capsicum spp.). Plant Breed. 128:701–706. DOI: 10.1111/j.1439-0523.2008.01615.x.
[CrossRef] [Google Scholar]
Mahasuk P., Struss D., Mongkolporn O. 2016. QTLs for resistance to anthracnose identified in two Capsicum sources. Mol. Breed. 36:10. DOI: 10.1007/s11032-016-0435-5.
[CrossRef] [Google Scholar]
Mahasuk P., Taylor PWJ., Mongkolporn O. 2009b. Identification of two new genes conferring resistance to Colletotrichum acutatum in Capsicum baccatum. Phytopathology. 99:1100–1104. DOI: 10.1094/PHYTO-99-9-1100. PMID: 19671013.
[CrossRef] [Google Scholar]
Mallard S., Cantet M., Massire A., Bachellez A., Ewert S., Lefebvre . 2013. A key QTL cluster is conserved among accessions and exhibits broad-spectrum resistance to Phytophthora capsici: a valuable locus for pepper breeding. Mol. Breed. 32:349–364. DOI: 10.1007/s11032-013-9875-3.
[CrossRef] [PDF] [Google Scholar]
Mammadov J., Aggarwal R., Buyyarapu R., Kumpatla S. 2012. SNP markers and their impact on plant breeding. Int. J. Plant Genomics. 728398. DOI: 10.1155/2012/728398. PMID: 23316221. PMCID: PMC3536327.
[CrossRef] [Google Scholar]
Matsunaga H., Saito T., Hirai M., Nunome T., Yoshida T. 2003. DNA markers linked to pepper mild mottle virus (PMMoV) resistant locus (L4) in Capsicum. J. Jpn. Soc. Hortic. Sci. 72:218–220. DOI: 10.2503/jjshs.72.218.
[CrossRef] [Google Scholar]
Mimura Y., Kageyama T., Minamiyama Y., Hirai M. 2009. QTL analysis for resistance to Ralstonia solanacearum in Capsicum accession 'LS2341'. J. Jpn. Soc. Hortic. Sci. 78:307–313. DOI: 10.2503/jjshs1.78.307.
[CrossRef] [Google Scholar]
Mimura Y., Yoshikawa M. 2009. Pepper accession LS2341 is highly resistant to Ralstonia solanacearum strains from Japan. HortScience. 44:2038–2040. DOI: 10.21273/HORTSCI.44.7.2038.
[CrossRef] [Google Scholar]
Min WK., Ryu JH., Ahn SH. 2014. Developmental changes of recessive genes-mediated Cucumber mosaic virus (CMV) resistance in peppers (Capsicum annuum L.). Korean J. Hortic. Sci. Technol. 32:235–240. DOI: 10.7235/hort.2014.13092.
[CrossRef] [PDF] [Google Scholar]
Minamiyama Y., Tsuro M., Kubo T., Hirai M. 2007. QTL analysis for resistance to Phytophthora capsici in pepper using a high density SSR-based map. Breed. Sci. 57:129–134. DOI: 10.1270/jsbbs.57.129.
[CrossRef] [Google Scholar]
Mishra B., Rout E., Mohanty JN., Joshi RK. 2019. Sequence-tagged site-based diagnostic markers linked to a novel anthracnose resistance gene RCt1 in chili pepper (Capsicum annuum L.). 3 Biotech. 9:9. DOI: 10.1007/s13205-018-1552-0. PMID: 30622847. PMCID: PMC6312824.
[CrossRef] [Google Scholar]
Mongkolporn O., Taylor PWJ. 2018. Chili anthracnose: Colletotrichum taxonomy and pathogenicity. Plant Pathol. 67:1255–1263. DOI: 10.1111/ppa.12850.
[CrossRef] [Google Scholar]
Monroy-Barbosa A., Bosland PW. 2008. Genetic analysis of phytophthora root rot race-specific resistance in chile pepper. J. Am. Soc. Hortic. Sci. 6:825–829. DOI: 10.21273/JASHS.133.6.825.
[CrossRef] [Google Scholar]
Moury B., Palloix A., Selassie KG., Marchoux G. 1997. Hypersensitive resistance to tomato spotted wilt virus in three Capsicum chinense accessions is controlled by a single gene and is overcome by virulent strains. Euphytica. 94:45–52. DOI: 10.1023/A:1002997522379.
[CrossRef] [Google Scholar]
Moury B., Pflieger S., Blattes A., Lefebvre V., Palloix A. 2000. A CAPS marker to assist selection of tomato spotted wilt virus (TSWV) resistance in pepper. Genome. 43:137–142. DOI: 10.1139/g99-098. PMID: 10701122.
[CrossRef] [Google Scholar]
Murphy JF., Blauth JR., Livingstone KD., Lackney VK., Jahn MK. 1998. Genetic mapping of the pvr1 locus in Capsicum spp. and evidence that distinct potyvirus resistance loci control responses that differ at the whole plant and cellular levels. Mol. Plant Microbe Interact. 11:943–951. DOI: 10.1094/MPMI.1998.11.10.943.
[CrossRef] [Google Scholar]
Ogundiwin EA., Berke TF., Massoudi M., Black LL., Huestis G., Choi D, et al. 2005. Construction of 2 intraspecific linkage maps and identification of resistance QTLs for Phytophthora capsici root-rot and foliar-blight diseases of pepper (Capsicum annuum L.). Genome. 48:698–711. DOI: 10.1139/g05-028. PMID: 16094437.
[CrossRef] [Google Scholar]
Pakdeevaraporn P., Wasee S., Taylor PWJ., Mongkolporn O. 2005. Inheritance of resistance to anthracnose caused by Colletotrichum capsici in Capsicum. Plant Breed. 124:206–208. DOI: 10.1111/j.1439-0523.2004.01065.x.
[CrossRef] [Google Scholar]
Park SK., Kim SH., Park HG., Yoon JB. 2009. Capsicum germplasm resistant to pepper anthracnose differentially interact with Colletotrichum isolates. Hortic. Environ. Biote. 50:17–23.
[Google Scholar]
Peeters N., Guidot A., Vailleau F., Valls M. 2013. Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era. Mol. Plant Pathol. 14:651–662. DOI: 10.1111/mpp.12038. PMID: 23718203. PMCID: PMC6638647.
[CrossRef] [Google Scholar]
Peterson BK., Weber JN., Kay EH., Fisher HS., Hoekstra HE. 2012. Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One. 7:e37135. DOI: 10.1371/journal.pone.0037135. PMID: 22675423. PMCID: PMC3365034.
[CrossRef] [Google Scholar]
Pflieger S., Lefebvre V., Caranta C., Blattes A., Goffinet B., Palloix A. 1999. Disease resistance gene analogs as candidates for QTLs involved in pepper-pathogen interactions. Genome. 42:1100–1110. DOI: 10.1139/g99-067. PMID: 10659776.
[CrossRef] [Google Scholar]
Phan NT., Sim SC. 2017. Genomic tools and their implications for vegetable breeding. Hortic. Sci. Technol. 35:149–164. DOI: 10.12972/kjhst.20170018.
[CrossRef] [Google Scholar]
Pierre M., Noël L., Lahaye T., Ballvora A., Veuskens J., Ganal M, et al. 2000. High-resolution genetic mapping of the pepper resistance locus Bs3 governing recognition of the Xanthomonas campestris pv vesicatora AvrBs3 protein. Theor. Appl. Genet. 101:255–263. DOI: 10.1007/s001220051477.
[CrossRef] [PDF] [Google Scholar]
Pinar H., Mutlu N., Ozaslandan A., Argun D., Keles D., Canhilal R. 2016. Reliability assessment of molecular markers linked to resistance genes against Meloidogyne spp. in diverse peppers genotypes. Egypt. J. Biol. Pest Co. 26:515–521.
[Google Scholar]
Pinto CMF., Santos IC., de Araujo., de Silva. do Rêgo ER., do Rego MM., Finger FL., editors2016. Pepper importance and growth (Capsicum spp.). Production and breeding of chilli peppers (Capsicum spp.). Springer Nature Switzerland AG;Switzerland: p. 1–25. DOI: 10.1007/978-3-319-06532-8_1.
[CrossRef] [Google Scholar]
Poland JA., Rife TW. 2012. Genotyping-by-sequencing for plant breeding and genetics. Plant Genome. 5:92–102. DOI: 10.3835/plantgenome2012.05.0005.
[CrossRef] [Google Scholar]
Quirin EA., Ogundiwin EA., Prince JP., Mazourek M., Briggs MO., Chlanda TS, et al. 2005. Development of sequence characterized amplified region (SCAR) primers for the detection of Phyto.5.2, a major QTL for resistance to Phytophthora capsici Leon. In pepper. Theor. Appl. Genet. 110:605–612. DOI: 10.1007/s00122-004-1874-7. PMID: 15657741.
[CrossRef] [PDF] [Google Scholar]
Rafalski A. 2002. Applications of single nucleotide polymorphisms in crop genetics. Curr. Opin. Plant Biol. 5:94–100. DOI: 10.1016/S1369-5266(02)00240-6. PMID: 11856602.
[CrossRef] [Google Scholar]
Rahman MS., Akanda AM., Mian IH., Bhuiyan MKA., Hossain MM. 2016. New sources of resistance to Cucumber mosaic virus in Capsicum annuum. J. Crop Sci. Biotech. 19:249–258. DOI: 10.1007/s12892-016-0044-1.
[CrossRef] [PDF] [Google Scholar]
Rehrig WZ., Ashrafi H., Hill T., Prince J., van Deynze. 2014. CaDMR1 cosegregates with QTL Pc5.1 for resistance to Phytophthora capsici in pepper (Capsicum annuum). Plant Genome. 7:1–12. DOI: 10.3835/plantgenome2014.03.0011.
[CrossRef] [Google Scholar]
Rezende JF., Leite ME., Nogueira DW., Nogueira DG., da Silva., Maluf WR. 2019. A new resistance gene to PepYMV (Pepper yellow mosaic virus) in Capsicum annuum L. Plant Breed. 139:65–72. DOI: 10.1111/pbr.12752.
[CrossRef] [Google Scholar]
Ribaut JM., Hoisington D. 1998. Marker-assisted selection: new tools and strategies. Trends Plant Sci. 3:236–239. DOI: 10.1016/S1360-1385(98)01240-0.
[CrossRef] [Google Scholar]
Ro NY., Hur OS., Ko HC., Kim SG., Rhee JH., Gwag JG, et al. 2012. Evaluation of resistance in pepper germplasm to Cucumber mosaic virus by high resolution melting analysis. Res. Plant Dis. 18:290–297. DOI: 10.5423/RPD.2012.18.4.290.
[CrossRef] [PDF] [Google Scholar]
Römer P., Hahn S., Jordan T., Straub T., Bonas U., Lahaye T. 2007. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science. 318:645–648. DOI: 10.1126/science.1144958. PMID: 17962564.
[CrossRef] [Google Scholar]
Römer P., Jordan T., Lahaye T. 2010. Identification and application of a DNA-based marker that is diagnostic for the pepper (Capsicum annuum) bacterial spot resistance gene Bs3. Plant Breed. 129:737–740. DOI: 10.1111/j.1439-0523.2009.01750.x.
[CrossRef] [Google Scholar]
Roossinck MJ. 2001. Cucumber mosaic virus, a model for RNA virus evolution. Mol. Plant Pathol. 2:59–63. DOI: 10.1046/j.1364-3703.2001.00058.x. PMID: 20572992.
[CrossRef] [Google Scholar]
Rubio M., Caranta C., Palloix A. 2008. Functional markers for selection of potyvirus resistance alleles at the pvr2-eIF4E locus in pepper using tetra-primer ARMS-PCR. Genome. 51:767–771. DOI: 10.1139/G08-056. PMID: 18772955.
[CrossRef] [Google Scholar]
Ruffel S., Gallois JL., Moury B., Robaglia C., Palloix A., Caranta C. 2006. Simultaneous mutations in translation initiation factors eIF4E and eIF(iso)4E are required to prevent pepper veinal mottle virus infection of pepper. J. Gen. Virol. 87:2089–2098. DOI: 10.1099/vir.0.81817-0. PMID: 16760413.
[CrossRef] [Google Scholar]
Seo E., Kim S., Yeom SI., Choi D. 2016. Genome-wide comparative analyses reveal the dynamic evolution of nucleotide-binding leucin-rich repeat gene family among Solanaceae plants. Front. Plant Sci. 7:1205. DOI: 10.3389/fpls.2016.01205. PMID: 27559340. PMCID: PMC4978739.
[CrossRef] [Google Scholar]
Shehzadi A., Abbas HMK., Ahmed Z., Saleem S. 2017. Effect plant disease resistance genes: Recent applications and future perspectives. J. Innov. Bio-Res. 1:86–103.
[Google Scholar]
Shin J., Xu SJ., Kim JY., Woo J., Kim HG., Hong ., SJ , et al. 2013. CMV-P1 resistance evaluation using enzyme-linked immunosorbent assay of pepper genetic sources (Capsicum spp.). Korean J. Hortic. Sci. Technol. 31:764–771. DOI: 10.7235/hort.2013.13021.
[CrossRef] [PDF] [Google Scholar]
Siddique MI., Lee HY., Ro NY., Kan K., Venkatesh J., Solomon AM, et al. 2019. Identifying candidate genes for Phytophthora capsici resistance in pepper (Capsicum annuum) via genotyping-by-sequencing-based QTL mapping and genome-wide association study. Sci. Rep. 9:9962. DOI: 10.1038/s41598-019-46342-1. PMID: 31292472. PMCID: PMC6620314.
[CrossRef] [Google Scholar]
Srivastava A., Mangal M. Ramchiary N., Kole C., editors2019. Capsicum breeding: history and development. The Capsicum Genome, Compendium of Plant Genomes. Springer Nature Switzerland AG;Switzerland: p. 25–55. DOI: 10.1007/978-3-319-97217-6_3. PMID: 30484737.
[CrossRef] [Google Scholar]
Stall RE., Jones JB., Minsavage GV. 2009. Durability of resistance in tomato and pepper to Xanthomonads causing bacterial spot. Annu. Rev. Phytopathol. 47:265–284. DOI: 10.1146/annurev-phyto-080508-081752. PMID: 19400644.
[CrossRef] [Google Scholar]
Sugita T., Yamaguchi K., Kinoshita T., Yuji K., Sugimura Y., Nagata R, et al. 2006. QTL analysis for resistance to Phytophthora blight (Phytophthora capsici Leon.) using an intraspecific doubled-haploid population of Capsicum annuum. Breed. Sci. 56:137–145. DOI: 10.1270/jsbbs.56.137.
[CrossRef] [Google Scholar]
Sugita T., Yamaguchi K., Sugimura Y., Nagata R., Yuji K., Kinoshita T, et al. 2004. Development of SCAR markers linked to L3 gene in Capsicum. Breed. Sci. 54:111–115. DOI: 10.1270/jsbbs.54.111.
[CrossRef] [Google Scholar]
Sun CY., Mao SL., Zhang ZH., Palloix A., Wang LH., Zhang BX. 2015. Resistances to anthracnose (Colletotrichum acutatum) of Capsicum mature green and ripe fruit are controlled by a major dominant cluster of QTLs on chromosome P5. Sci. Hortic. 181:81–88. DOI: 10.1016/j.scienta.2014.10.033.
[CrossRef] [Google Scholar]
Sun X., Liu D., Zhang X., Li W., Liu H., Hong W, et al. 2013. SLAF-seq: An efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS One. 8:e58700. DOI: 10.1371/journal.pone.0058700. PMID: 23527008. PMCID: PMC3602454.
[CrossRef] [Google Scholar]
Suwor P., Sanitchon J., Thummabenjapone P., Kumar S., Techawongstien S. 2017. Inheritance analysis of anthracnose resistance and marker-assisted selection in introgression populations of chili (Capsicum annuum L.). Sci. Hortic. 220:20–26. DOI: 10.1016/j.scienta.2017.03.032.
[CrossRef] [Google Scholar]
Suwor P., Thummabenjapone P., Sanitchon J., Kumar S., Techawongstien S. 2015. Phenotypic and genotypic responses of chili (Capsicum annuum L.) progressive lines with different resistant genes against anthracnose pathogen (Colletotrichum spp.). Eur. J. Plant Pathol. 143:725–736. DOI: 10.1007/s10658-015-0723-7.
[CrossRef] [PDF] [Google Scholar]
Suzuki K., Kuroda T., Miura Y., Murai J. 2003. Screening and field trials of virus resistant sources in Capsicum spp. Plant Dis. 87:779–783. DOI: 10.1094/PDIS.2003.87.7.779. PMID: 30812886.
[CrossRef] [Google Scholar]
Tai T., Dahlbeck D., Stall RE., Peleman J., Staskawicz BJ. 1999a. High-resolution genetic and physical mapping of the region containing the Bs2 resistance gene of pepper. Theor. Appl. Genet. 99:1201–1206. DOI: 10.1007/s001220051325.
[CrossRef] [PDF] [Google Scholar]
Tai T., Staskawicz BJ. 2000. Construction of a yeast artificial chromosome library of pepper (Capsicum annuum L.) and identification of clones from the Bs2 resistance locus. Theor. Appl. Genet. 100:112–117. DOI: 10.1007/s001220050016.
[CrossRef] [PDF] [Google Scholar]
Tai TH., Dahlbeck D., Clark ET., Gajiwala P., Pasion R., Whalen MC, et al. 1999b. Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc. Natl. Acad. Sci. U.S.A. 23:14153–14158. DOI: 10.1073/pnas.96.24.14153. PMID: 10570214. PMCID: PMC24206.
[CrossRef] [Google Scholar]
Thabuis A., Palloix A., Pflieger S., Daubèze AM., Caranta C., Lefebvre V. 2003. Comparative mapping of Phytophthora resistance loci in pepper germplasm: evidence for conserved resistance loci across Solanaceae and for a large genetic diversity. Theor. Appl. Genet. 106:1473–1485. DOI: 10.1007/s00122-003-1206-3. PMID: 12750791.
[CrossRef] [PDF] [Google Scholar]
Thabuis A., Palloix A., Servin B., Daubèze AM., Signoret P., Hospital F, et al. 2004. Marker-assisted introgression of 4 Phytophthora capsici resistance QTL alleles into a bell pepper line: validation of additive and epistatic effects. Mol. Breed. 14:9–20. DOI: 10.1023/B:MOLB.0000037991.38278.82.
[CrossRef] [Google Scholar]
Thakur PP., Mathew D., Nazeem PA., Abida PS., Indira P., Girija D, et al. 2014. Identification of allele specific AFLP markers linked with bacterial wilt [Ralstonia solanacearum (Smith) Yabuuchi.] resistance in hot peppers (Capsicum annuum L.). Physiol. Mol. Plant P. 87:19–24. DOI: 10.1016/j.pmpp.2014.05.001.
[CrossRef] [Google Scholar]
Thomson MJ. 2014. High-throughput SNP genotyping to accelerate crop improvement. Plant Breed. Biotech. 2:195–212. DOI: 10.9787/PBB.2014.2.3.195.
[ScienceCentral] [CrossRef] [PDF] [Google Scholar]
Tomita R., Murai J., Miura Y., Ishihara H., Liu S., Kubotera Y, et al. 2008. Fine mapping and DNA fiber FISH analysis locates the tobamovirus resistance gene L3 of Capsicum chinense in a 400-kb region of R-like genes cluster embedded in highly repetitive sequences. Theor. Appl. Genet. 117:1107–1118. DOI: 10.1007/s00122-008-0848-6. PMID: 18663424. PMCID: PMC2755798.
[CrossRef] [PDF] [Google Scholar]
Tomita R., Sekine KT., Mizumoto H., Sakamoto M., Murai J., Kiba A, et al. 2011. Genetic basis for the hierarchical interaction between Tobamovirus spp. and L resistance gene alleles from different pepper species. Mol. Plant Microbe Interact. 24:108–117. DOI: 10.1094/MPMI-06-10-0127. PMID: 20879841.
[CrossRef] [Google Scholar]
Tran NH., Kim BS. 2010. Inheritance of resistance to bacterial wilt (Ralstonia solanacearum) in pepper (Capsicum annuum L.). Hortic. Environ. Biote. 51:431–439.
[Google Scholar]
Tran PT., Choi H., Choi D., Kim KH. 2015. Molecular characterization of Pvr9 that confers a hypersensitive response to Pepper mottle virus (a potyvirus) in Nicotiana benthamiana. Virology. 481:113–123. DOI: 10.1016/j.virol.2015.02.052. PMID: 25776758.
[CrossRef] [Google Scholar]
Truong HTH., Kim JH., Cho MC., Chae SY., Lee HE. 2013. Identification and development of molecular markers linked to Phytophthora root rot resistance in pepper (Capsicum annuum L.). Eur. J. Plant Pathol. 135:289–297. DOI: 10.1007/s10658-012-0085-3.
[CrossRef] [PDF] [Google Scholar]
Truong HTH., Kim KT., Kim DW., Kim S., Chae Y., Park JH, et al. 2012. Identification of isolate-specific resistance QTLs to phytophthora root rot using an intraspecific recombinant inbred line population of pepper (Capsicum annuum). Plant Pathol. 61:48–56. DOI: 10.1111/j.1365-3059.2011.02483.x.
[CrossRef] [Google Scholar]
Truong HTH., Kim KT., Kim S., Cho MC., Kim HR., Woo JG. 2011. Development of gene-based markers for the Bs2 bacterial spot resistance gene for marker-assisted selection in pepper (Capsicum spp.). Hortic. Environ. Biote. 52:65–73. DOI: 10.1007/s13580-011-0142-4.
[CrossRef] [PDF] [Google Scholar]
Tsuda S., Kirita M., Watanabe Y. 1998. Characterization of a pepper mild mottle tobamovirus strain capable of overcoming the L3 gene-mediated resistance, distinct from the resistance-breaking Italian isolate. Mol. Plant Microbe Interact. 11:327–331. DOI: 10.1094/MPMI.1998.11.4.327. PMID: 9530869.
[CrossRef] [Google Scholar]
Uncu AT., Celik I., Devran Z., Ozkaynak E., Frary A., Frary A, et al. 2015. Development of a SNP-based CAPS assay for the Me1 gene conferring resistance to root knot nematode in pepper. Euphytica. 206:393–399. DOI: 10.1007/s10681-015-1489-x.
[CrossRef] [PDF] [Google Scholar]
Vallejos CE., Jones V., Stall RE., Jones JB., Minsavage GV., Schultz DC, et al. 2010. Characterization of two recessive genes controlling resistance to all races of bacterial spot in peppers. Theor. Appl. Genet. 121:37–46. DOI: 10.1007/s00122-010-1289-6. PMID: 20180094.
[CrossRef] [PDF] [Google Scholar]
van der., Jones JDG. 1998. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23:454–456. DOI: 10.1016/S0968-0004(98)01311-5. PMID: 9868361.
[CrossRef] [Google Scholar]
van Eck. 2018. Genome editing and plant transformation of solanaceous food crops. Curr. Opin. Biotech. 49:35–41. DOI: 10.1016/j.copbio.2017.07.012. PMID: 28800419.
[CrossRef] [Google Scholar]
Varshney RK., Nayak SN., May GD., Jackson SA. 2009. Next-generation sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol. 27:522–530. DOI: 10.1016/j.tibtech.2009.05.006. PMID: 19679362.
[CrossRef] [Google Scholar]
Venkatesh J., An J., Kang WH., Jahn M., Kang BC. 2018. Fine mapping of the dominant potyvirus resistance gene Pvr7 reveals a relationship with Pvr4 in Capsicum annuum. Phytopathology. 108:142–148. DOI: 10.1094/PHYTO-07-17-0231-R. PMID: 28945517.
[CrossRef] [Google Scholar]
Venkatesh J., Jahn M., Kang BC. 2016. Genome-wide analysis and evolution of the Pto-like protein kinase (PLPK) gene family in pepper. PLoS One. 11:e0161545. DOI: 10.1371/journal.pone.0161545. PMID: 27536870. PMCID: PMC4990186.
[CrossRef] [Google Scholar]
Voorrips RE., Finkers R., Sanjaya L., Groenwold R. 2004. QTL mapping of anthracnose (Colletotrichum spp.) resistance in a cross between Capsicum annuum and C. chinense. Theor. Appl. Genet. 109:1275–1282. DOI: 10.1007/s00122-004-1738-1. PMID: 15309301.
[CrossRef] [PDF] [Google Scholar]
Wang J., Lin M., Crenshaw A., Hutchinson A., Hicks B., Yeager M, et al. 2009. High-throughput single nucleotide polymorphism genotyping using nanofluidic Dynamic Arrays. BMC Genomics. 10:561. DOI: 10.1186/1471-2164-10-561. PMID: 19943955. PMCID: PMC2789104.
[CrossRef] [Google Scholar]
Wang P., Wang L., Guo J., Yang W., Shen H. 2016. Molecular mapping of a gene conferring resistance to Phytophthora capsici Leonian race 2 in pepper line PI201234 (Capsicum annuum L.). Mol. Breed. 36:66. DOI: 10.1007/s11032-016-0464-0.
[CrossRef] [Google Scholar]
Wang X., Fazari A., Cao Y., Zhang Z., Palloix A., Mao S, et al. 2018. Fine mapping of the root-knot nematode resistance gene Me1 in pepper (Capsicum annuum L.) and development of markers tightly linked to Me1. Mol. Breed. 38:39. DOI: 10.1007/s11032-018-0793-2.
[CrossRef] [Google Scholar]
Wiesner-Hanks T., Nelson R. 2016. Multiple disease resistance in plants. Annu. Rev. Phytophathol. 54:229–252. DOI: 10.1146/annurev-phyto-080615-100037. PMID: 27296142.
[CrossRef] [Google Scholar]
Xu X., Chao J., Cheng X., Wang R., Sun B., Wang H, et al. 2016. Mapping of a novel race specific resistance gene to phytophthora root rot of pepper (Capsicum annuum) using bulked segregant analysis combined with specific length amplified fragment sequencing strategy. PLoS One. 11:e0151401. DOI: 10.1371/journal.pone.0151401. PMID: 26992080. PMCID: PMC4798474.
[CrossRef] [Google Scholar]
Xu Y., Li P., Yang Z., Xu C. 2017. Genetic mapping of quantitative trait loci in crops. Crop J. 5:175–184. DOI: 10.1016/j.cj.2016.06.003.
[CrossRef] [Google Scholar]
Yang HB., Liu WY., Kang WH., Jahn M., Kang BC. 2009. Development of SNP markers linked to the L locus in Capsicum spp. by a comparative genetic analysis. Mol. Breed. 24:433–446. DOI: 10.1007/s11032-009-9304-9.
[CrossRef] [PDF] [Google Scholar]
Yang HB., Liu WY., Kang WH., Kim JH., Cho HJ., Yoo JH, et al. 2012. Development and validation of L allele-specific markers in Capsicum. Mol. Breed. 30:819–829.
[CrossRef] [PDF] [Google Scholar]
Yao M., Li N., Wang F., Ye Z. 2013. Genetic analysis and identification of QTLs for resistance to cucumber mosaic virus in chili pepper (Capsicum annuum L.). Euphytica. 193:135–145. DOI: 10.1007/s10681-013-0953-8.
[CrossRef] [PDF] [Google Scholar]
Yeam I., Kang BC., Lindeman W., Frantz JD., Faber N., Jahn MM. 2005. Allele-specific CAPS markers based on point mutations in resistance alleles at the pvr1 locus encoding eIF4E in Capsicum. Theor. Appl. Genet. 112:178–186. DOI: 10.1007/s00122-005-0120-2. PMID: 16283234.
[CrossRef] [PDF] [Google Scholar]
Yin K., Gao C., Qiu JL. 2017. Progress and prospects in plant genome editing. Nature Plants. 3:17107. DOI: 10.1038/nplants.2017.107. PMID: 28758991.
[CrossRef] [PDF] [Google Scholar]
Yoon JB., Yang DC., Lee WP., Ahn SY., Park HG. 2004. Genetic resources resistant to anthracnose in the genus Capsicum. J. Korean Soc. Hortic. Sci. 45:318–323.
[Google Scholar]

Fig. 1
Position of disease resistance genes or QTLs on the pepper reference genome (Capsicum annuum cv. CM334 v1.55; http://peppergenome.snu.ac.kr; Kim et al. 2014). Bs3, Bacterial spot 3 (Römer et al. 2007); Cmr1, Cucumber mosaic resistance 1 (Kang et al. 2010); qCmr2.1, QTL Cucumber mosaic resistance 2.1 (Guo et al. 2017a); pvr6, potyvirus resistance 6 (Ruffel et al. 2006); PMR1, Powdery Mildew Resistance 1 (Jo et al. 2017); pvr1, potyvirus resistance 1 (Kang et al. 2005); pvr2, potyvirus resistance 2 (Kang et al. 2005); LtR4.2, Leveillula taurica resistance 4.2 (Kim et al. 2017a); Phyto5.2, QTL phytophthora resistance 5.2 (Quirin et al. 2005); Pc5.1, QTL Phytophthora capsici 5.1 (Mallard et al. 2013); CaPhyto, QTL Capsicum Phytophthora (Wang et al. 2016); AnR5, QTL Anthracnose Resistance 5 (Sun et al. 2015); Pvr9, Potyvirus resistance 9 (Tran et al. 2015); bs5, bacterial spot 5 (Vallejos et al. 2010); Lt_6.1, QTL Leveillula taurica 6.1 (Lefebvre et al. 2003); cmr2, cucumber mosaic resistance 2 (Choi et al. 2018); Bw1, Bacterial wilt 1 (Mimura et al. 2009); Bs2, Bacterial spot 2 (Tai et al. 1999b); Me gene cluster, Me1, Me3, Me4, Me7, Mech1, Mech2, and N genes (Fazari et al. 2012); CcR9, QTL Colletotrichum capsici Resistance 9 (Lee et al. 2011); qRRs-10.1, QTL Resistance Ralstonia solanacearum 10.1 (Du et al. 2019); PhR10, QTL Phytophthora Resistance 10 (Xu et al. 2016); Tsw, Tomato spotted wilt resistance (Kim et al. 2017c); Pvr4, Potyvirus resistance 4 (Kim et al. 2017c); Pvr7, Potyvirus resistance 7 (Venkatesh et al. 2018); RCt1, QTL Resistance Colletotrichum truncatum 1 (Mishra et al. 2019); Phyt-3, QTL Phytophthora 3 (Sugita et al. 2006); qcmv11.1 and qcmv11.2, QTL cucumber mosaic virus 11.1 and 11.2 (Li et al. 2018); L, resistance locus to tobamoviruses (Tomita et al. 2008); qcmv12.1, QTL cucumber mosaic virus 12.1 (Li et al. 2018); CaR12.2, QTL Colletotrichum acutatum Resistance 12.2 (Lee et al. 2011).
PBB-8-077-f1.tif
Table 1
Molecular markers linked to the genes or QTLs resistant to fungal diseases in pepper.
Group Disease Pathogen Resistance locus Chr. Marker or gene Type of marker Population Inheritance pattern Status of research Reference

Parents Generation Number of plants
Fungi Anthracnose Colletotrichum scovillei (formerly C. acutatum) CaR12.2 12 CaR12.2M1-CAPS CAPS ‘SP26’ × ‘PBC81’ BC1F2 87 QTL Genetic mapping Lee et al. 2011
Co5 4 BACSNP-4-63, -60 SNP ‘PBC80’ × ‘CA1316’ F2 146 QTL Genetic mapping Mahasuk et al. 2016
AnR5 5 InDel, HpmsE116 InDel, SSR ‘77013’ × ‘PBC932’ BC1 186 QTL Genetic mapping Sun et al. 2015
CaR12.2 12 SCAR-Indel, HpmsE032 SCAR, SSR ‘PS’ × ‘PR1’, ‘PS’ × ‘PR2 F2, BC1 468 Single dominant Marker analysis Suwor et al. 2017
Colletotrichum truncatum (formerly C. capsici) CcR9 9 CcR9M1-SCAR SCAR ‘SP26’ × ‘PBC81’ BC1F2 87 QTL Genetic mapping Lee et al. 2011
co1, co2 2 CAP_T22290_0_1_429, CAP_T39318_0_1_1042 SNP ‘Bangchang’ × ‘PBC932’ F2 126 QTL Genetic mapping Mahasuk et al. 2016
RCt1 11 CtR-431, CtR-594 STS ‘Punjab Lal’ × ‘Arka Lohit’ F2, BC1 354 Single dominant Genetic mapping Mishra et al. 2019
Powdery mildew Leveillula taurica Lt_6.1 6 E36/M59-380h AFLP ‘H3’ × ‘Vania’ DH 101 QTL Genetic mapping Lefebvre et al. 2003
Lt_9.1 9 D11_0.8h RAPD ‘H3’ × ‘Vania’ DH 101 QTL Genetic mapping Lefebvre et al. 2003
LtR4.2 4 Ltr4.1-40344, Ltr4.2-56301, Ltr4.2-585119 SNP ‘SP26’ × ‘PBC81’ BC1F2 87 QTL Marker analysis Kim et al. 2017a
PMR1 4 ZL1_1826, HPGV_1313, HPGV_1344, HPGV_1412, KS16052G01 SCAR, SNP ‘VK515R’ × ‘VK515S’ F2:3 102 Single dominant Candidate gene identification Jo et al. 2017
Cultivar ‘PM Singang’ F2 80
Table 2
Molecular markers linked to the genes or QTLs resistant to Phytophthora capsici in pepper.
Group Disease Pathogen Resistance locus Chr. Marker or gene Type of marker Population Inheritance pattern Status of research Reference
Population
Parents Generation Number of plants
Oomycetes Phytophthora root rot Phytophthora capsici Phyto5.2 5 D04.717-SCAR SCAR ‘CM334’ × ‘Yolo B’ F3 families 9 families Single dominant Marker development Quirin et al. 2005
CAMS420 SSR ‘Manganji’ × ‘CM334’ DH 96 QTL Genetic mapping Minamiyama et al. 2007
P5-SNAP SNAP ‘CM334’ × ‘Chilsungcho’ F2 100 QTL Marker development Kim et al. 2008b
M3-CAPS CAPS ‘Subicho’ × ‘CM334’ F2 96 Single dominant Marker development Lee et al. 2012b
SA133_4, UBC553 SCAR, RAPD ‘YCM334’ × ‘Tean’ RIL 126 Single dominant Marker development Truong et al. 2013
Phyto5NBS1 SNP ‘YCM334’ × ‘Tean’ RIL 128 Single dominant Candidate gene identification Liu et al. 2014
Pc5.1 5 CA036100, CA004482 SNP ‘H3’ × ’Vania’ DH 101 QTL Candidate gene identification Mallard et al. 2013, Rehrig et al. 2014
‘Perennial’ × ‘Yolo Wonder’ DH 114
‘Yolo Wonder’ × ‘CM334’ RIL 297
CaPhyto 5 ZL6726, ZL6970 SSR ‘Shanghaiyuan’ × ‘PI201234’ F2 794 QTL Candidate gene identification Wang et al. 2016
Phyt-1 5 M10E3-6 AFLP ‘K9-11’ × ‘AC2258’ DH 176 QTL Genetic mapping Sugita et al. 2006
Phyt-2 1 RP13-1 RAPD ‘K9-11’ × ‘AC2258’ DH 176 QTL Genetic mapping Sugita et al. 2006
Phyt-3 11 M9E3-11 AFLP ‘K9-11’ × ‘AC2258’ DH 176 QTL Genetic mapping Sugita et al. 2006
PhR10 10 P52-11-21, P52-11-41 SSR ‘CM334’ × ‘NMCA10399’ F2, BC1 853 Single dominant Candidate gene identification Xu et al. 2016
QTL5.1, QTL5.2, QTL5.3 5 EC5-bin27 SNP ‘CM334’ × ‘ECW30R’ RIL 188 QTL Genetic mapping Siddique et al. 2019
S05_27703815
EC5-bin51
Table 3
Molecular markers linked to the genes or QTLs resistant to viruses in pepper.
Group Disease Pathogen Resistance locus Chr. Marker or gene Type of marker Population Inheritance pattern Status of research Reference
Population
Parents Generation Number of plants
Viruses CMV Cucumber mosaic virus CMV 12 A5.1 RAPD ‘Perennial’ × ‘Yolo Wonder’ DH 94 Single dominant Genetic mapping Pflieger et al. 1999
cmv11.1 11 E35/M48-101 AFLP ‘Maor’ × ‘Perennial’ F3 families 180 QTL Genetic mapping Ben Chaim et al. 2001
cmv12.1 12 E33/M48-132, E40/M47-262 AFLP ‘H3’ × ‘Vania’ DH 101 QTL Genetic mapping Caranta et al. 2002
Cmr1 2 CaTm-int3-HRM, CaT1616BAC, 240H02sp6 SNP Cultivar ‘Bukang’ F2 309 Single dominant Marker development Kang et al. 2010
qcmv.hb-8.2 11 UBC829 RAPD ‘BJ0747’ × ‘XJ0630’ F2, BC1 334 QTL Genetic mapping Yao et al. 2013
qCmr11.1 11 Indel-11-64 InDel ‘PBC688’ × ‘G29’ F2 289 QTL Candidate gene identification Guo et al. 2017a
qcmv11.1 11 Marker6201026 SNP ‘BJ0747’ × ‘XJ0630’ F2 195 QTL Genetic mapping Li et al. 2018
qcmv11.2 Marker5409028
qcmv12.1 Marker17652010
cmr2 8 Affy4, IBP160, cmvAFLP SNP ‘Lan32’ × ‘Jeju’ F2 129 Single recessive Genetic mapping Choi et al. 2018
Potyvirus Pepper mottle virus (PepMoV) pvr1 (= pvr2) 4 Pvr1-S, pvr1-R1, pvr1-R2 CAPS R and S accessions Line 23 Single recessive Marker development Yeam et al. 2005
eIF4E-A614G, -G325A, -T236G, -T200A ARMS-PCR ‘Yolo Wonder’ × ‘CM334’, ‘Perennial’ × ‘Yolo Y’, ‘Perennial’ × ‘Florida VR2’ F2 - Single recessive Marker development Rubio et al. 2008
KASP_pvr1 KASP ‘Habanero’ × ‘PI159234’ F2 56 Single recessive Marker development Holdsworth and Mazourek 2015
Pvr4 (= Pvr7) 10 Pvr4-CAPS CAPS ‘Yolo Wonder’ × ‘CM334’ F2 151 Single dominant Marker development Caranta et al. 1999
SCUBC19 SCAR ‘SCM334’ × ‘Yolo Wonder’ F2 110 Single dominant Marker development Arnedo-Andrés et al. 2002
HpmsE031 SSR ‘CM334’ × ‘Chilsungcho’ F2 100 Single dominant Genetic mapping Kim et al. 2011
MY1421 SNP ‘SR-231’ × ‘CM334’ F2 204 Single dominant Genetic mapping Devran et al. 2015
SNP-H2.4, SNP-H1.5, SNP-H1.6 (Pvr4 = Pvr7) SNP ‘9093’ × ‘Jeju’ F2 916 Single dominant Candidate gene identification Venkatesh et al. 2018
Pepper veinal mottle virus (PVMV) pvr6 3 eIF(iso)4E gene-based marker InDel ‘DH218’ × ‘F’ F2 182 Single recessive Gene cloned Ruffel et al. 2006
Chilli veinal mottle virus (ChiVMV) Pvr6-SCAR SCAR ‘Dempsey’ × ‘Perennial’ F2 187 Single recessive Marker development Hwang et al. 2009
Tobamovirus Pepper mild mottle virus (PMMoV) L3 11 21L24M, A339, 197AD5R, 253A1R SCAR, SNP ‘KOS’ × ‘NDN’ F2 3,391 Single dominant Define of cosegregating region Tomita et al. 2008
‘PI159236’ × ‘LS1839-2-4’ F2 2,016
L3, L4 11 L3-SCAR, L4-SCAR SCAR Cultivars F1 53 Single dominant Marker development Lee et al. 2012a
L3-HRM, L4-HRM SNP Cultivars ‘Special’, ‘Myoung-sung’ F2 631, 858 Single dominant Marker development Yang et al. 2012
TSWV Tomato spotted wilt virus Tsw 10 SCAC568 CAPS ‘Cupra’ × ‘Baltasar’ BC1-like 92 Single dominant Marker development Kim et al. 2008c
Table 4
Molecular markers linked to the genes or QTLs resistant to bacterial and nematode diseases in pepper.
Group Disease Pathogen Resistance locus Chr. Marker or gene Type of marker Population Inheritance pattern Status of research Reference
Population
Parents Generation Number of plants
Bacteria Bacterial spot Xanthomonas campestris pv. vesicatora Bs2 9 A2-SCAR, S19-SCAR SCAR ‘ECW’ × ‘ECW-123R’ F2, BC1 1577 Single dominant Genetic mapping Tai et al. 1999a
Bs3 2 P23-70, P22-3 AFLP Cultivars Line 17 Single dominant Fine mapping Pierre et al. 2000
B104SP6, B103T7 STS Cultivars Line 17 Single dominant Define of cosegregating region Jordan et al. 2006
PR-Bs3 InDel Accessions Line 19 Single dominant Marker development Römer et al. 2010
KASP_Bs3 KASP Accessions Line 25 Single dominant Marker development Holdsworth and Mazourek 2015
bs5 6 PepA2, PepC2, PepF4 AFLP ‘NuMex R Naky’ × ‘PI159234’ F2 100 Two recessive (bs5 and bs6) Genetic mapping Vallejos et al. 2010
Bacterial wilt Ralstonia solanacearum Bw1 8 CAMS451 SSR ‘LS2341’ × ‘CW’ DH 94 QTL Genetic mapping Mimura et al. 2009
qRRs-10.1 10 ID10-194305124 SNP ‘BVRC25’ × ‘BVRC1’ F2, BC1 504 QTL Candidate gene identification Du et al. 2019
Nematodes Root-knot nematode Meloidogyne spp.(M. incognita, M. javanica, M. arenaria) Me3, Me4 9 HM1, HM2, SSCP_B322 AFLP, SSCP ‘PM687’ × ‘Yolo Wonder’ DH 103 Single dominant Genetic mapping Djian-Caporalino et al. 2001
Me1, Mech2 9 SCAR_CD (PM54), SCAR_HM60, SCAR_PM54 SCAR ‘DH330’ × ‘DLL’ F2 373 Single dominant Genetic mapping Djian-Caporalino et al. 2007
Me7, Mech1 9 CAPS_F4R4 (HM58), Q04_0.3, SSCP_B322 (PM6) CAPS, RAPD, SSCP ‘DLL’ × ‘PM702’ F2 301 Single dominant Genetic mapping Djian-Caporalino et al. 2007
N 9 SCAR_PM6a, SCAR_PM6b, SSCP_PM5, SCAR_N SCAR, SSCP ‘CW’ × ‘20080-5-29’ F2 132 Single dominant Genetic mapping Fazari et al. 2012
CA_CAPS_2, CA_SSR37 CAPS, SSR ‘CW’ × ‘AZN-1’ F2 256 Single dominant Candidate gene identification Celik et al. 2016
Me1 9 CL000081-05555, C2At2g06530, CL001943-1222 CAPS, COSII ‘AZN-1’ × ‘PM217’ F2 100 Single dominant Marker development Uncu et al. 2015
16830-H-V2, 16830-CAPS HRM, CAPS ‘DH330’ × ‘0516’ BC1 1,598 Single dominant Fine mapping Wang et al. 2018
Me loci 9 SCAR_PM54 SCAR Accessions Line 14 Single dominant Validity test of marker Pinar et al. 2016
Me3 9 11F6F, 43N9R, Me3-F/R, 242G21R, 25F15F STS HDA149 Line 1 Single dominant Physical mapping Guo et al. 2017b
Me7 9 G24U5, SF164076, CA1-1b, 611109646, SCAR_PM6a, SCAR_PM6b, SF164024, SF16406, 2111b1 SNP, SCAR ‘ECW30R’ × ‘CM334’ F2 714 Single dominant Candidate gene identification Changkwian et al. 2019
Table 5
Cloned and candidate genes for pepper disease resistance.
Locus Chr. Encoding protein Gene name Resistance resource Reference
Bs2 9 nucleotide binding site–leucine-rich repeat (NLR) protein Bs2 C. chacoense ‘PI260435’ C. annuum ‘ECW-20R’ Tai et al. 1999b
pvr1 4 Eukaryotic translation initiation factor 4E (eIF4E) eIF4E C. chinense ‘PI152225’, ‘PI159234’, ‘PI159236’ Kang et al. 2005
pvr6 3 Eukaryotic translation initiation factor iso 4E (eIF(iso)4E) eIF(iso)4E C. annuum ‘Perennial’ Ruffel et al. 2006
Bs3 2 Flavin-dependent monooxygenase (FMOs) Bs3 C. annuum ‘PI271322’ C. annuum ‘ECW-30R’ Römer et al. 2007
L 11 coiled-coil, nucleotide-binding, leucine-rich repeat protein (CC-NB-LRR) L3 C. chinense ‘PI152225’ Tomita et al. 2011
Pc5.1 5 Homoserine kinase (HSK) CaDMR1 C. annuum ‘CM334’ Rehrig et al. 2014
Pvr9 6 CC-NB-ARC-LRR protein Pvr9 C. annuum ‘CM334’ Tran et al. 2015
CaPhyto 5 Leucine rich repeat receptor-like serine/threonine-protein kinase BRI1-like 2 (BRL2) Capana05g000764 C. annuum ‘PI201234’ Wang et al. 2016
Disease resistance protein RPP13 Capnan05g000769
Tsw 10 Nucleotide-binding and leucine-rich domain protein (NLR) CcNBARC575 C. chinense ‘PI159236’ Kim et al. 2017c
Pvr4 10 Nucleotide-binding and leucine-rich domain protein (NLR) CaNBARC322 C. annuum ‘CM334’ Kim et al. 2017c
qCmr2.1 2 N-like protein (TMV resistance protein) (TIR-NBS-ACR-LRR) CA02g19570 C. frutescens ‘PBC688’ Guo et al. 2017a
PMR1 4 NLR domain-containing R protein 408 and 556 C. annuum ‘VK515R’, C. annuum ‘PM Singang’ Jo et al. 2017
Me1 9 Putative late blight resistance protein (homolog with R1A-3 gene) CA09g16830 C. annuum ‘PI201234’ Wang et al. 2018
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