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.
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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 F
2 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 BC
1F
2 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 F
2 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, 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’ F
2 plants (
Jo et al. 2017). In addition to that, the report indicated that
PMR1 locus might have been introgressed from
C. baccatum.
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 F
1 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 F
2 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 F
2 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 (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 F
1 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 F
3 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 F
1 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 F
2 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).
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 P
0 pathotype viruses such as Tomato mosaic virus (ToMV);
L2 (
C. frutescens) confers resistance to P
0 and P
1 pathotype Paprika mild mottle virus (PaMMV) that overcomes
L1 resistance;
L3 (
C. chinense) confers resistance to P
0, P
1, and P
1,2 pathotype Pepper mild mottle virus (PMMoV) that overcomes
L2 resistance;
L4 (
C. chacoense) confers resistance to P
0, P
1, 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 F
2 population derived from a cross between ‘AP-PM04’ (resistant; derived from ‘PI260429’) and ‘Mie-midori’ (susceptible) (
Matsunaga et al. 2003). Three SCAR markers; PMFR11
269, PMFR11
283 and PMFR21
200, positioned at a distance of 4.0 cM from the
L3 locus, were developed from two RAPD markers, E18
272 and E18
286, which were developed by applying the BSA method to two DH populations, K9-DH and K9/AC-DH, derived from F
1 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 BC
4F
2 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 F
2 population (2,016 individuals) of
C. annuum (introduced from
C. chinense ‘PI152225’) and an interspecific F
2 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 F
2 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).
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, UBC19
1432 and SCUBC19
1432, 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 F
2 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 (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 SCAC
568 was developed from the OPAC10
593 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 SCAC
568 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-06
270 was identified using the segregating BC
4F
1 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 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 F
2 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).
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 F
2 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 F
2 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 P
0, P
1, and P
1,2 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).
Fig. 1Position 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 1Molecular 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 |
‘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 2Molecular 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 3Molecular 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 |
|
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 4Molecular 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
|
|
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 5Cloned 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
|
|
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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