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

Geleta Dugassa Barka; Jundae Lee

doi:10.9787/PBB.2020.8.2.89

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

Geleta Dugassa Barka, Jundae Lee^,*

Plant Breeding and Biotechnology 2020;8(2):89-113.
Published online: June 1, 2020

DOI: https://doi.org/10.9787/PBB.2020.8.2.89

Department of Horticulture, Institute of Agricultural Science & Technology, Jeonbuk National University, Jeonju 54896, Korea

*Corresponding author Jundae Lee, ajfall@jbnu.ac.kr, Tel: +82-63-270-2560, Fax: +82-63-270-2581

• Received: March 31, 2020 • Revised: May 15, 2020 • Accepted: May 15, 2020

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Abstract
INTRODUCTION
MARKER DEVELOPMENT FOR PEPPER DISEASE RESISTANCE
GENE CLONING FOR PEPPER DISEASE RESISTANCE
FUTURE PROSPECTS
CONCLUSION
ACKNOWLEDGEMENTS
References

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.
Key words: Disease resistance, Fine mapping, Introgression, Map-based cloning, QTL, Resistance gene

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, P_R1 derived from ‘PBC932’ and P_R2 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’ F_2:3 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 CMV_MES and CMV_N 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 CMV_Korean and CMV_FNY 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, CMV_P1 strain breaking the CMV_P0 resistance of pepper in the field was first reported in 2006 (Lee et al. 2006). A total of 10 CMV_P1-resistant peppers were identified by evaluating 199 pepper genetic resources using enzyme-linked immunosorbent assays (ELISA) (Shin et al. 2013). The CMV_P1 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 CMV_P1 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 CMV_P1 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 P_1,2 pathotype Pepper mild mottle virus (PMMoV) that overcomes L² resistance; L⁴ (C. chacoense) confers resistance to P₀, P₁, P_1,2, and P_1,2,3 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 P_1,2 pathotypes of Tobamovirus, was revealed by map-based cloning, while other alleles of the L locus, including L¹, L^1a, L^1c, L², L^2b, 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).

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).

Table 1

Molecular markers linked to the genes or QTLs resistant to fungal diseases in pepper.

Table 1
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	‘P_S’ × ‘P_R1’, ‘P_S’ × ‘P_R2’	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’	F_2:3	102	Single dominant	Candidate gene identification	, Jo et al. 2017
			PMR1	4	ZL1_1826, HPGV_1313, HPGV_1344, HPGV_1412, KS16052G01	SCAR, SNP	Cultivar ‘PM Singang’	F₂	80	Single dominant	Candidate gene identification	, Jo et al. 2017

Table 2

Molecular markers linked to the genes or QTLs resistant to Phytophthora capsici in pepper.

Table 2
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.

Table 3
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
		qcmv12.1	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	3	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
			L3	11	21L24M, A339, 197AD5R, 253A1R	SCAR, SNP	‘PI159236’ × ‘LS1839-2-4’	F₂	2,016	Single dominant	Define of cosegregating region	, Tomita et al. 2008
			L3, L4	11	L3-SCAR, L4-SCAR	SCAR	Cultivars	F1	53	Single dominant	Marker development	, Lee et al. 2012a
			L3, L4	11	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.

Table 4
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
	Bacterial wilt	Ralstonia solanacearum	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
			N	9	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
			Me1	9	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.

Table 5
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
CaPhyto	5	Disease resistance protein RPP13	Capnan05g000769	C. annuum ‘PI201234’	, Wang et al. 2016
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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Molecular Marker Development and Gene Cloning for Diverse Disease Resistance in Pepper (Capsicum annuum L.): Current Status and Prospects

Plant Breed. Biotech.. 2020;8(2):89-113. Published online June 1, 2020

DOI: https://doi.org/10.9787/PBB.2020.8.2.89

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

Plant Breed. Biotech.. 2020;8(2):89-113. Published online June 1, 2020

DOI: https://doi.org/10.9787/PBB.2020.8.2.89

Figure

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

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).

Fig. 1

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

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	‘P_S’ × ‘P_R1’, ‘P_S’ × ‘P_R2’	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’	F_2:3	102	Single dominant	Candidate gene identification	Jo et al. 2017
			PMR1	4	ZL1_1826, HPGV_1313, HPGV_1344, HPGV_1412, KS16052G01	SCAR, SNP	Cultivar ‘PM Singang’	F₂	80	Single dominant	Candidate gene identification	Jo et al. 2017

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
		qcmv12.1	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	3	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
			L3	11	21L24M, A339, 197AD5R, 253A1R	SCAR, SNP	‘PI159236’ × ‘LS1839-2-4’	F₂	2,016	Single dominant	Define of cosegregating region	Tomita et al. 2008
			L3, L4	11	L3-SCAR, L4-SCAR	SCAR	Cultivars	F1	53	Single dominant	Marker development	Lee et al. 2012a
			L3, L4	11	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
	Bacterial wilt	Ralstonia solanacearum	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
			N	9	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
			Me1	9	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
CaPhyto	5	Disease resistance protein RPP13	Capnan05g000769	C. annuum ‘PI201234’	Wang et al. 2016
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

Table 1 Molecular markers linked to the genes or QTLs resistant to fungal diseases in pepper.

Table 2 Molecular markers linked to the genes or QTLs resistant to Phytophthora capsici in pepper.

Table 3 Molecular markers linked to the genes or QTLs resistant to viruses in pepper.

Table 4 Molecular markers linked to the genes or QTLs resistant to bacterial and nematode diseases in pepper.

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

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Abstract

INTRODUCTION

MARKER DEVELOPMENT FOR PEPPER DISEASE RESISTANCE

GENE CLONING FOR PEPPER DISEASE RESISTANCE

FUTURE PROSPECTS

CONCLUSION

ACKNOWLEDGEMENTS

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