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Perspective

Resistance to Anthracnose Rot Disease in Capsicum

by
Lei Cui
1,2,
Michiel C. van den Munckhof
2,
Yuling Bai
2 and
Roeland E. Voorrips
2,*
1
College of Agriculture, Shanxi Agricultural University, Taiyuan 030031, China
2
Plant Breeding, Wageningen University & Research, P.O. Box 386, 6700 AJ Wageningen, The Netherlands
*
Author to whom correspondence should be addressed.
Agronomy 2023, 13(5), 1434; https://doi.org/10.3390/agronomy13051434
Submission received: 14 April 2023 / Revised: 9 May 2023 / Accepted: 14 May 2023 / Published: 22 May 2023
(This article belongs to the Special Issue New Insights into Pathogen, Insect Pest, and Weed Control in Field and Greenhouse Cropping Systems)
Browse Figures
Versions Notes

Abstract

:
Pepper (Capsicum spp.) is an important vegetable crop worldwide with high economic and nutritional value. The Capsicum genus comprises more than 30 species, of which C. annuum, C. chinense, C. baccatum, C. frutescens, and C. pubescens are the five domesticated ones. Anthracnose fruit rot, caused by Colletotrichum spp., is one of the most destructive fungal diseases of pepper. In this review, we compiled up-to-date information from 40 publications on anthracnose resistance in Capsicum species. In total, 375 accessions were described as showing different levels of resistance against Colletotrichum spp. These accessions belonged to different species, including C. annuum (160), C. baccatum (86), C. chacoense (4), C. chinense (90), and C. frutescens (16), as well as 19 accessions of which the species were not reported. High levels of resistance were mainly present in C. baccatum and C. chinense. For some of the resistant accessions, resistance genes or quantitative trait loci (QTL) were reported. Using associated molecular markers, we located 31 QTLs and 17 resistance-related genes in the recently published Capsicum genomes, including C. annuum CM334 version 1.6, C. chinense version 1.2, and C. baccatum version 1.2. Our results could be helpful for making use of some reported accessions in the breeding of pepper cultivars with resistance to anthracnose rot disease.

1. Introduction

The Capsicum species, or pepper, is commonly used as a vegetable and a spice. The economic importance of pepper is highlighted by its global annual production in 2017 of approximately 31.5 million tons for fresh pepper and 3.6 million tons for dried pepper [1]. Although pepper originates from South America, most of the world’s production currently takes place in Asia, which contributes to more than 65% of the total.
Capsicum belongs to the Solanaceae family. Currently, 38 Capsicum species are recognized, including the five important domesticated species: C. annuum, C. baccatum, C. chinense, C. frutescens, and C. pubescens [2,3]. The Capsicum species is diploid (n = 12). Its genome is, in general, quite complex, and contains a large amount of repetitive DNA sequences, which has resulted in genome sizes above 3 Gb [4,5]. Because of the large genome size, the development of reference sequences has been delayed compared with other Solanaceous crops, for instance, tomato (900 Mb, Tomato Genome Consortium) [6] and potato (844 Mb, Potato Genome Sequencing Consortium) [7]. Until now, five Capsicum genomes have been completely sequenced, of which three are C. annuum and the others are C. baccatum and C. chinense [4,5,8]. The five pepper genomes are C. annuum cv. CM334 (3.06 Gb with 34,903 annotated genes); cv. Zunla-1 (3.35 Gb), a wild accession Chiltepin of C. annuum var. glabriusculum (3.48 Gb); C. baccatum PBC81 (3.9 Gb); and C. chinense PI 159236 (3.2 Gb).
Anthracnose is a major disease of pepper caused by a complex of Colletotrichum species, mainly occurring in the (sub-)tropics during the wet season. The prevalence of anthracnose is usually associated with a high amount of inoculum in the soil, which is the primary source of infection. Secondary spread occurs rapidly through conidial dispersion in air or surface water, or even by insects such as fruit flies (Dacus spp.) [9,10]. Colletotrichum is able to infect pepper plants at all developmental stages. The major species causing anthracnose in seedlings, leaves, and stems is C. coccodes [11,12]. The most prevalent and virulent species causing fruit rot are C. scovillei (previously known as C. acutatum), C. siamense (previously known as C. gloeosporioides), and C. truncatum (previously known as C. capsici) [13,14,15,16,17]. The taxonomy of Colletotrichum species has recently been revised based on pathogenicity and multi-gene phylogenetic analyses [18]. Typical anthracnose fruit rot symptoms, found on both green and ripe fruit, are black sunken necrotic tissues with water-soaked rings of wet acervuli [19] (Figure 1), leading to a loss of market value. The annual yield loss of pepper due to anthracnose has been reported to vary from 10% [20] to 50% [21], and can sometimes even be as high as 80% [22].
Control measures against anthracnose include the application of chemical fungicides, seed sterilization or cleaning, crop rotation, and biological control [23,24]. The frequent application of fungicides leads to environmental pollution and promotes the development of fungicide-resistant Colletotrichum strains [25,26]. As an alternative, growing resistant cultivars is considered to be the most effective and economic method to combat this disease. However, unlike for several other major pepper diseases, no commercial anthracnose-resistant cultivars have been released. The main factor that hinders anthracnose resistance breeding is the polygenic nature of the resistance and large variation in pathotypes [27]. Nevertheless, a vast number of Capsicum accessions have been evaluated worldwide, and anthracnose resistance has been identified in domesticated species including C. annuum, C. baccatum, C. chinense, and C. frutescens [28,29,30,31]. In addition, a few accessions from the wild species C. chacoense were reported to be resistant [30]. Genetic studies on some of these resistant accessions have identified monogenic (both dominantly and recessively inherited) and polygenic factors contributing to resistance, with the latter representing the most common type of resistance [15,21,25,26,28,32,33,34].
As many of these genetic studies were performed prior to the release of the genome sequences, the locations of the genes/quantitative trait loci (QTLs) were not reported in relation to a common genome or map, and are hence hard to compare. Therefore, we aimed to provide a comprehensive overview of current knowledge on anthracnose resistance in pepper in terms of the source and genetics of the identified resistance, as well as the chromosomal locations of the reported anthracnose resistance genes and QTLs. This effort could provide a new starting point for making use of the identified resistant sources in breeding programs.

2. Bioassays for Evaluating Anthracnose Resistance

A key factor for success in breeding for anthracnose resistance is the methods used for inoculation and evaluation. Inoculation can be performed on fruits, either detached or still on the plant, or on whole plants (Table 1). To determine foliar resistance, pepper plants at various growth stages have been inoculated with conidial suspension via foliar spray [35,36]. For fruit bioassays, two approaches are widely used: the fruit is either not wounded or wounded prior to inoculation [19,37]. The wound inoculation ensures direct entry of the spores without considering the cuticle and epidermis as the primary defense barrier [25,38]. This can be achieved either via a so-called pinprick method [39,40] or via a microinjection procedure [16,41]. Non-wound inoculation delivers the conidia spores onto the fruit either via droplets (detached fruits) or via spraying (in planta or detached) [42,43].
Most screening studies have been based on bioassays of detached fruits at different maturity stages, mainly the mature green and ripe stages (Table 1). In Capsicum species, fruit maturity is a well-documented factor that influences the expression of anthracnose resistance. Genetic analyses in populations derived from C. chinense PBC932 and C. baccatum PBC80 have revealed that resistance in mature green and ripe fruit is controlled by different genes [22,28,43,44]. Mongkolporn et al. [44] reported that detached fruits of accession PBC932 at the mature green stage were more resistant than at the ripening stage. Two linked genes are responsible for resistance at the mature green and ripe fruit stages [22]. In contrast, the ripe fruit of accession PBC80 was more resistant than the mature green fruit [28,43]. In PBC80, resistance at the ripe fruit stage is controlled by a dominant gene, while an independent recessive gene mediates resistance in mature green fruit [28,43].
For evaluating anthracnose resistance, various assessment methods have been used by different research groups (Table 1). For example, a high resistance score has been based on four aspects: low incidence (the proportion of diseased plants/fruits of the total number of plants/fruits assessed) [39,45], low severity (lesion size as a proportion of fruit size) [31,36,46], low infection rate (the fraction of inoculations resulting in a lesion) [26,47], and low AUDPC value (the area under the disease progress curve) [16,48]. In some studies, different aspects are combined. For example, disease severity and incidence were converted to the disease severity index [44,49,50,51], while in other studies, lesion diameter was measured as well as the infection rate [25], disease incidence [26], and AUDPC [48].
Table
Table 1. Inoculation and evaluation methods used in previous studies to evaluate anthracnose resistance and susceptibility.
Table 1. Inoculation and evaluation methods used in previous studies to evaluate anthracnose resistance and susceptibility.
Pathogen a Bioassay b Inoculation Method c Disease Evaluation Method d Phenotypic Responses e Reference
C. scovillei11DSIR (1–<3); IR (3–<6); S (6–9)[52]
21/2DSIHR (0); R (0.1–1.9); MR (2.0–2.9); S (3.0–4.9); HS (5)[30]
44Infection rateR (infection rate < 10%)[53]
33DIHR (0–<10%); R (10–<20%); MR (20–<40%); S (40–<70%); HS (>70%)[45]
33DSI, AUDPC, IP, LPR (low value for AUDPC, and high values for IP and LP)[16]
33DSIHR (1); R (3); MR (4); MS (6); S (8); HS (10)[41]
C. brevisporum53DSI based on LSR (<10%); MR (11–20%); S (21–40%); HS (>41%)[36]
61DSI based on LS (foliar)1 (SL); 2 (>1 mm); 3 (1%); 4 (5%); 5 (10%); 6 (25%)[36]
C. capsici72DSI based on LSR (0–1.0); MR (1.1–2.0); MS (2.1–3.0); S (3.1–4.0); HS (4.1–5.0)[40]
-4DSI based on DII (0%); R (1–5%); MR (6–25%); S (26–50%); HS (51–100%)[51]
71DSI based on LSR (<20%); MR (21–40%); MS (41–60%); S (>60%)[46]
61/2DSI based on LSSL (0); R (0.1–10%); MR (10.1–25%); MS (25.1–50%); S (50.1–75%); HS (75.1–100%)[31]
C. coccodes61/5DSI and AUDPCIndex (0–5)[54]
C. siamense33DSIHR (1); R (3); MR (4); MS (6); S (8); HS (10)[55]
C. siamense86/3DSI and AUDPCHR (1); R (3); MR (4); MS (6); S (8); HS (10)[48]
C. capsid, C. siamense72DSI based on DII (0); R (1); MR (2); S (3); HS (4)[39]
C. scovillei23Lesion diameter and infection frequency [26,47]
C. capsici, C. siamense32 [25]
C. siamense23LI [56]
C. scovillei, C. capsici, C. siamense, C. truncatum81/3DSI based on LSHR (0); R (1); MR (3); MS (5); S (7); HS (9)[28,44,49,50,57]
Colletotrichum spp. 31DI, lesion diameter, LGR, AUDPC, IPR (low values for AUDPC, DI, lesion diameter, and LGR; high values for IP)[58]
a C. scovillei (previously known as C. acutatum), C. siamense (previously known as C. gloeosporioides), and C. truncatum (previously known as C. capsici). b 1: detached immature green fruit; 2: detached mature green fruit; 3: detached mature green and ripe fruits; 4: immature green and ripe red fruits on plants; 5: detached (im)mature fruits; 6: chili plants; 7: detached ripe fruits; 8: unripe and ripe fruit detached/on plants. c 1: spray; 2: pinpricking wounding; 3: microinjection; 4: natural field inoculation; 5: soil-drench method; 6: dropping spores on the pericarp. d Disease incidence (DI): percentage of fruit infected with inoculation sites at which lesion diameter > 4 mm; lesion growth rate (LGR): the measurement of lesion growth over time and calculated in mm/day; incubation period (IP) and latent period (LP): the number of days from inoculation to the appearance of symptoms; lesion incidence (LI): percentage of inoculation sites at which lesions ≤ 4 mm in diameter; percent lesion size (LS): lesion size as a proportion of fruit size; DSI: disease severity index; AUDPC: area under the disease progress curve. e Codes are interpreted from the original studies. Immune: I; symptomless: SL; highly resistant: HR; resistant: R; intermediate resistance: IR; moderately resistant: MR; susceptible: S; highly susceptible: HS. Between brackets, the original phenotypic classes or measurements are shown.

3. Sources of Anthracnose Resistance in Capsicum Germplasm

Breeding for resistance to anthracnose in pepper was started in the early 1990s by Korean and Indian chili breeders [59]. Their breeding programs mainly relied on moderate resistance obtained from C. annuum sources (cv. Perennial and Chungryong), which is the most widely cultivated Capsicum species [59,60]. Aiming to identify resistance at a high level, disease tests have been performed worldwide in a large number of Capsicum accessions. In total, 375 resistant accessions have been identified in the cultivated Capsicum species corresponding to C. annuum (160), C. baccatum (86), C. chinense (90), and C. frutescens (16) as well as in the wild species C. chacoense (4) and 19 accessions of unreported species [28,29,30,31] (Table 2 and Table S1).
In these screening, six Colletotrichum species were used, of which three (C. scovillei, C. truncatum, and C. siamense) are prevalent worldwide and three (C. coccodes, C. brevisporum, and C. dematium) are common in Asia [19]. In most of the screens, a single Colletotrichum species was used. In a few cases, C. annuum accessions were evaluated against multiple Colletotrichum spp., leading to the identification of 18 accessions with broad resistance (Table 2).
In order to avoid redundant screenings in future studies, we summarize and present accessions identified as susceptible (Table S2). This panel included 255 accessions of the following species: C. annuum (167 accessions), C. baccatum (31), C. chinense (38), and C. frutescens (19).

4. Breeding for Anthracnose Resistance in Capsicum

Some of the resistant accessions of C. annuum, C. baccatum, and C. chinense listed in Table 2 have been used as donors for anthracnose resistance (Table 3). However, the resistance identified in C. baccatum is difficult to transfer into elite C. annuum lines, as an interspecific crossing barrier exists between both species [52]. As a result, one or multiple bridge crosses or embryo rescues are necessary in order to introgress the resistance into C. annuum [67]. For example, hybrids of C. baccatum PBC80 with elite C. annuum cultivars have been obtained with the aid of embryo rescue [71]. On the other hand, resistance in the accessions of C. annuum and C. chinense is generally easier to introduce into existing C. annuum lines.
The development of resistant cultivars can be facilitated with prior knowledge of the genetic basis of resistance and associated molecular markers for marker-assisted selection (MAS). The very first genetic map of anthracnose resistance in pepper was derived from an interspecific population between C. annuum and a resistant C. chinense accession, PRI95030 [25] (Table 3). More recent genetic maps have been constructed and genetic analysis has been conducted in several populations derived from the main resistance sources, including C. chinense PBC932 [15]; C. baccatum PBC80 [34], PBC81 [29,72], PI594137 [47], and 881045 (Cbp) [33]. In addition, genetic studies have also been based on resistance obtained from C. annuum sources including cv. Perennial, cv. Chungryong, cv. Punjab Lal, and accessions 83–168, which are not highly resistant (Table 3). Results from these genetic studies indicate that the estimated inheritance of resistance depends not only on the Colletotrichum species and methods used for inoculation, but also on the fruit stages and the other parental lines used in the study (Table 3). For example, a single recessive gene model was suggested for the resistance of C. chinense PBC932 against C. truncatum (previously known as C. capsici) infection at different maturity stages in a cross with C. annuum cv. Bangchang (Table 3) [22], while polygenic resistance against C. scovillei was found at the mature green and ripe fruit stages in crosses between PBC 932 and C. annuum 9955-15 [72] or 77013 [15]. The inheritance of Colletotrichum spp. resistance derived from C. baccatum accessions PBC80, PBC81, and PI594137, from either intraspecific populations or an interspecific cross with C. annuum, was shown to be controlled by single or multiple genes at different maturity stages [28,29,43,47]. In contrast, monogenic resistance was found to be responsible for resistance to C. truncatum (previously known as C. capsici) in C. annuum accessions 83–168 [73], and to C. scovillei in C. baccatum accessions PI594137 [47] and PBC80 [34].
To introgress anthracnose resistance into a C. annuum line, backcrossing is one of the most important techniques used in breeding [74]. Successful resistant lines have been obtained from the backcrossing of resistant sources of C. baccatum and C. chinense with a recurrent elite C. annuum cultivar. At the AVRDC (the World Vegetable Center), five C. annuum lines, namely AVPP1102-B, AVPP0513, AVPP0719, AVPP0207, and AVPP1004-B, were found to be promising in terms of fruit yield and tolerance to anthracnose [45]. Two C. annuum varieties from IVEGRI (the Indonesian Vegetables Research Institute), Lembang-1 and Tanjung-2, have been reported to possess moderate resistance [75]. There have been multiple anthracnose-resistant C. annuum lines reported in India, including PBC-380, BS-20, BS28, Taiwan-2, Pant C-1 [31], LLS, VI047018 (derived from C. chinense PBC932), Breck-2, VI046804 (derived from C. baccatum PBC80), Breck-1, Jaun, and VI046805 (derived from C. baccatum PBC81) [76].
Table
Table 3. Capsicum accessions used in anthracnose resistance breeding.
Table 3. Capsicum accessions used in anthracnose resistance breeding.
Genetic SourceResistance Level aPopulationColletotrichum spp. bInoculation MethodGenetic Mechanism cReference
Capsicum spp.AccessionTypeSusceptible ParentMature GreenRipe
C. annuumChungryongMRF2, BC1C. annuum PI244670C. dematium, C. siamenseDetached pinprickingPartial dominant *Partial dominant *[59,68]
PerennialMRF2, BC1, BC2C. annuum ‘Kolascai E-14’C. truncatum-Polygenicna[60,68]
83–168MRF2, BC1C. annuum ‘KKU-Cluster’C. capsiciDetached dropping Single dominantna[73]
Punjab LalRF2C. annuum ‘PT 12-3’C. scovillei, C. capsiciDetached pinprickingPolygenicPolygenic[77]
GBUEL104HRF2, BC1, BC2C. annuum GBUEL103C. scovilleiDetached microinfectionTwo dominant QTLs *Two dominant QTLs *[41]
C. chinensePRI95030HRF2C. annuum ‘Jatilaba’C. siamense, C. capsiciDetached pinprickingnaPolygenic [25]
PBC932RF2, BC1, BC3C. annuum ‘9955-15’C. scovilleiDetached microinfectionTwo dominant genes *Polygenic recessive *[72]
PBC932HRF2, BC1C. annuum ‘Yeoju’, ‘Bangchang’C. capsiciSingle recessive *Single recessive *[22,26]
PBC932RBC1C. annuum ‘77013’C. scovilleiPolygenic dominant *Polygenic dominant *[15]
C. baccatumPI594137RF2, BC1C. baccatum Golden-ajiC. scovilleiDetached microinfectionSingle dominantna[47]
PBC80HRF2, BC1C. baccatum CA1316C. scovilleiSingle recessive *Single dominant *[28,34,43]
PBC81HRF2, BC1C. annuum SP26, MatikasC. scovillei, C. capsiciPolygenic *Polygenic *[29,78]
881045 (Cbp)RF2C. baccatum Golden-ajiC. scovilleinaPolygenic[33]
a Highly resistant: HR; resistant: R; moderate resistance: MR. b C. scovillei (previously known as C. acutatum), C. siamense (previously known as C. gloeosporioides), and C. truncatum (previously known as C. capsici). c * resistance in mature green and ripe fruit controlled by distinct genes; na: genetic information not available as mapping has not been performed.

5. Location of Anthracnose Resistance on the Pepper Genome

Knowledge on the localization of resistance genes and QTLs is of utmost importance when it comes to the development of markers linked to the resistance, subsequent gene introgression, and identification of allelic variants present in novel (wild) material. Many studies have been devoted to this aim, and their output, including resistant sources, Colletotrichum strains, linkage maps, and linked/flanking markers, is summarized in Table S3. However, for many of the genes and QTLs reported to date, their localization on the corresponding genome is not available due to the lack of reference sequences at the time of their first report. With the availability of the three pepper genomes [4,5,8], we attempted to map previously reported genes and QTLs on the chromosomes (Table 4 and Table S3, Figure 2). After retrieving the reported sequences of associated markers, primer pairs, fragments, and genes, in silico mapping was performed on the corresponding genomes (C. annuum CM334 version 1.6, C. chinense version 1.2, or C. baccatum version 1.2) using BLASTN (nucleotide-to-nucleotide BLAST) in TBtools software [79]. For BLASTN, sequences of two categories were used. The first category is for AFLP markers and other PCR markers for which sequences of the amplified fragments are known. Amplicon sequences (>100 bp) were used, and the chromosome with the most likely hit (E-value below 1 × 10−5) was chosen. The second category is for when the amplicon sequences are unknown. Primer sequences of about 20 bp were used and the setting was then set for short query sequences with an E-value threshold of 1000. When multiple markers could be used for one QTL, the chromosome anchored by the majority of markers was chosen. Some QTLs could not be anchored since their flanking markers had hits on different chromosomes.
In total, 56 QTLs were reported from 11 studies (Table 4), and 31 of them were anchored using the in silico mapping approach. The BLAST hits (markers flanking and/or within the QTL regions) were found across all 12 Capsicum spp. chromosomes (Table 4 and Table S3, Figure 2).
In the C. chinense accession PBC932, a major QTL for resistance to C. scovillei on the bottom of chromosome 5 was consistently detected in different studies [80,81,82,83]. The interval is flanked by the markers P5in-2266-404 and P5in-2268-978 within a physical distance of 164 kb in the physical map [82]. Additionally, many other QTLs were identified in the study of Sun et al. [15], of which four were likely located on chromosomes 3 (AnRGo12), 5 (AnRGO5_AnRGT5), 7 (AnRgo7), and 10 (AnRGo10/AnRGD10). For resistance to C. capcisi, three QTLs were found, with two of them mapped to chromosomes 9 (QTLUL) and 11 (QTL-L4) [84].
In C. baccatum PBC80, monogenic resistance to C. truncatum (previously known as C. capsici) was found that could be inherited either dominantly or recessively [22,26]. In the study of Suwor et al. [81], a major contributing QTL (LG12) against C. scovillei was identified that could be anchored to chromosome 12.
In C. baccatum PBC81, many QTLs were identified in three independent studies [72,85,86]. In the study of Lee et al. [86], one QTL (CcR9) for resistance to C. truncatum (previously known as C. capsici) could be mapped to chromosome 3, while the other one (CaR12.2) for resistance against C. scovillei could be mapped to chromosome 12. Three QTLs (RA80f6_r1, RA80f6_g1, and RA80f6_g2) conferring C. scovillei resistance were mapped to chromosomes 4, 8, and 3, respectively [72].
In C. baccatum var. pendulum 881045, Kim et al. [33] found more than 15 QTLs contributing the resistance to C. scovillei. A major QTL, An9.1, could be mapped to the top of chromosome 1. A few minor QTLs could be assigned to chromosomes 3 (An8.1/An8.2), 4 (An4.1), 6 (An7.2–7.4), and 10 (An 13.1).
In C. chinese PRI195030, four QTLs were detected [25], of which only two could be mapped, including the QTLs H1 on chromosome 2 for C. scovillei resistance and B1 on chromosome 7 for resistance to C. truncatum (previously known as C. capsici) and C. scovillei. Other QTLs could not be assigned to any chromosomes since their associated markers are mapped to different chromosomes.
Table
Table 4. Published QTL studies on anthracnose resistance.
Table 4. Published QTL studies on anthracnose resistance.
Study QTLFlanking Marker(s)LOD aR2 bIn Silico Mapping ChromosomeColletotrichum SpeciesResistant SourceFruit Stage cTrait d
Capsicum SpeciesAccession
[25]B1E37M51_184cCD3.9–9.316.3–77.17C. capsici, C. scovilleiC. chinensePRI95030FLA, IF
B2P11M49_355cCD_352jCD2.7–4.730.2–51.81C. scovillei
P11M51_362j2
E37M51_184cCD7
E37M51_251j10
P11M51_28012
H1P11M51_362j2.9–3.713.4–20.52
G1P11M50_137j, P14M58_199jCD 2.87.6-C. capsiciLD
[85]QTL_LG1hpms1-166, hpms1-274 7C. scovilleiC. baccatumPBC81GF, RFDI, TLD
hpms1-155 8
QTL_LG7hpms2-24 -
QTL_LG9hpms1-216, hpms1-274 -
QTL_LG10AF039662 -
[84]QTL-ULG31 9C. capsiciC. chinensePBC932GFLA
QTL_L4G28 11
QTL_L3G41 -
[33]An9.1E1174.614.41C. scovilleiC. baccatum var. pendulum881045FDA
An8.1-8.2E9464–4.12–8.43
An8.1-8.2E9464–4.12–8.43DR
An4.1E15403.10.64-
An7.2-7.4E672, E3842.5–3.84.9–37.56DR
An13.1E2462.915.410DA
An3.1-3.3 E63M82_270, E65M81_4502.7–3.612.8–30.1-DR
An5.1E74M79_370, E77M81_3202.93.9-
[33]An6.1me02em03_04, me02em02_052.80.9-C. scovilleiC. baccatum var. pendulumFDR
An7.1E76M83_250, E65M80_4203.411.3-DA
An7.5E77M83_320, E75M83_4503.96.9-DR
An8.3E70M84_380, E71M79_2953.315.2-
An8.4E71M79_330, E67M79_2503.820.5-
An9.2E76M83_350, E75M81_480310.8-DA
[29]CaR12.2CaR12.2M1_A_CAPS7.8–9.611.9–20.51C. scovilleiC. baccatumPBC81GF, RFTLD
CaR12.2M1_B_CAPS12
CcR9HpmsE14313.4–15.957.5–78.93C. capsiciDI, TLD, OLD
CaR12.1EtagMcag11, EtccMcga054.717.9-C. scovilleiRFTLD
CcRCEaacMcgc02, EaatMccg076.710.6-C. capsiciDI
[77]QTL_LG1EPMS725_HPMS7253.4–5.816.7–711C. scovilleiC. annuumPunjab LalGF, RFIP
HPMSE0163
QTL_LG2HPMSE0512.1–4.97.2–189
QCcR-ifp-iivr-1.1
QCcG-la.iivr1.1		CAMS020, HPMSE016 HPMS725, CAMS6443.514.2-C. capsiciIP, LA
[80]QTL_ARA518_InDel_98b, A518_seq_281b,
A518_primer_89c		5C. scovilleiC. chinensePBC932GFOLD
[15]AnRGO3HpmsE1262.32.93C. scovilleiC. chinensePBC932GFOLD
ES3824
AnRGO12ES64, Epms7452.73.13
AnRGO5_AnRGT5InDel-HpmsE116, InDel31.9–32.360.5–62.45OLD, TLD
AnRGO7HpmsE0572.22.57OLD
AnRGO10, AnRGD10C2_At4g03400, Gp200682.2–2.32.9–4.710OLD, DI
AnRGD5, AnRRO5, AnRRT5, AnRRD5HpmsE1162.7–12.39.3–33.2-GF, RFDI, OLD, TLD
AnRGD12ES118, ES1812.85.4-GFDI
[81]P.5SCAR-InDel 5C. scovilleiC. chinensePBC932GFLD
LG12SSR-HpmsE032 12C. baccatumPBC80
[82]AnRGO5P5in-2266-404,
P5in-2268-978		24.469.35C. scovilleiC. chinensePBC932GFTLD
[72]RA80f6_r1SNP_305/331417.74C. scovilleiC. baccatumPBC81GF, RFIP
RA80f6_g1SNP_541/5715.220.28
RA80f6_g2SNP_228/2183.512.83
a LOD: likelihood of odds ratio; b R2: percentage of phenotypic variance explained by each QTL; c GF: green fruit, RF: red fruit, F: fruit (undefined); d DI: disease incidence, TLD: true lesion diameter, OLD: overall lesion diameter, IP: Infection percentage, LA: lesion area, DR: disease rate, DA: disease area, IF: infection frequency.
Agronomy 13 01434 g002a 550Agronomy 13 01434 g002b 550Agronomy 13 01434 g002c 550Agronomy 13 01434 g002d 550
Figure 2. Anthracnose resistance-associated QTLs, genes, and fragments projected on the physical chromosomes of C. annuum CM334 version 1.6, C. chinense version 1.2, and C. baccatum version 1.2. Positions are in million base pairs. QTLs and genes are displayed as bars or indicators shown to the right of the chromosomes. Their names as given by the authors are maintained, and the study from which they originate is indicated between brackets. Molecular markers flanking the QTLs are indicated on the corresponding chromosomes. Synteny links are represented by black lines. Depending on the origin of resistance sources, molecular markers, QTLs, and genes are displayed in different colors (i.e., red for C. annuum, green for C. chinense, and blue for C. baccatum). Information was visualized using MapChart 2.3 [87]. (A) Physical maps of chromosomes 1–3 of C. annuum CM334 version 1.6, C. chinense version 1.2, and C. baccatum version 1.2; (B) physical maps of chromosomes 4–6; (C) physical maps of chromosomes 7–9; (D) physical maps of chromosomes 10–12.
Figure 2. Anthracnose resistance-associated QTLs, genes, and fragments projected on the physical chromosomes of C. annuum CM334 version 1.6, C. chinense version 1.2, and C. baccatum version 1.2. Positions are in million base pairs. QTLs and genes are displayed as bars or indicators shown to the right of the chromosomes. Their names as given by the authors are maintained, and the study from which they originate is indicated between brackets. Molecular markers flanking the QTLs are indicated on the corresponding chromosomes. Synteny links are represented by black lines. Depending on the origin of resistance sources, molecular markers, QTLs, and genes are displayed in different colors (i.e., red for C. annuum, green for C. chinense, and blue for C. baccatum). Information was visualized using MapChart 2.3 [87]. (A) Physical maps of chromosomes 1–3 of C. annuum CM334 version 1.6, C. chinense version 1.2, and C. baccatum version 1.2; (B) physical maps of chromosomes 4–6; (C) physical maps of chromosomes 7–9; (D) physical maps of chromosomes 10–12.
Agronomy 13 01434 g002aAgronomy 13 01434 g002bAgronomy 13 01434 g002cAgronomy 13 01434 g002d
In C. annuum PT-12-3, among the four reported QTLs, only QTL_LG2 could be assigned to chromosome 9 [68].

6. Defense Mechanisms of Anthracnose Resistance Caused by Colletotrichum spp.

The complete resistance of C. chinense accession PBC932 and C. baccatum accessions PBC80 and PBC81 is due to a hypersensitive reaction (HR) [12,22,28]. The immune response consists of slight tissue necrosis and localized cell death surrounding the inoculation site on the detached fruits [22,28,88]. The infected cells themselves have thickened cell walls or a thickened cuticle layer and have high levels of reactive oxygen species [12,88].
To understand the molecular mechanisms of defense against anthracnose, differential Capsicum spp.–Colletotrichum spp. pathosystems have been used to evaluate the expression of defense-related genes or the production of antimicrobial compounds. Based on an expression study with the C. truncatum-resistant accession Bhut Jolokia (obtained from a cross between C. frutescens and C. chinense), Mishra et al. [89] identified a number of defense-related genes, including PDF1.2, lipoxygenase Lox3, PR2, PR5, and transcription factors (WRKY33 and CaMYB), as possibly being involved in the resistance response.
In C. baccatum accession PBC80, pathogen-responsive gene 10 (PR10) was differentially expressed upon C. scovillei infection [90]. This gene is located on C. baccatum chromosome 2 at 78.2 Mb. In C. baccatum accession P27 challenged with Colletotrichum spp., the resistant response was dependent on the ripening stage and correlated with the accumulation of the metabolites butane-2,3-diol, fructose, and phenolics, and superoxide dismutase and peroxidase activities [58].
In the incompatible interaction of C. annuum cv. Nokkwang with C. siamense, six defense-responsive genes, including cytochrome P450, a PepCYP gene, a thionin-like gene (PepThi), a defensin gene (J1-1) [91], a pepper thaumatin-like gene (PepTLP), a MADS-box gene (PepMADS) [92], and a pepper esterase gene (PepEST) [93], were reported, of which PepCYP was mapped towards the bottom of chromosome 11, PepThi on the distal top of chromosome 7, J1-1 on the top of chromosome 8, PepTLP on chromosome 1 at 5.08 Mb, PepMADS on chromosome 11 at 14.7 Mb, and PepEST on chromosome 4 at 208.98 Mb. Moreover, the salicylic acid-induced protection of ripe pepper fruits of cv. Nokkwang against C. siamense was associated with highly expressed SA-responsive genes (SRGs) [94]. A SRG, namely BJ03029B07, was located at the top of C. annuum chromosome 6, and BJ03028G01 was located towards the bottom of this chromosome. Additionally, BJ03028G01 co-localized with QTL An7.2–7.4. The possible involvement of these genes in anthracnose resistance controlled by the QTL An7.2–7.4 needs to be studied. In C. annuum cv. Hanbyul, a systemic acquired resistance gene (CASAR8.2) with three cDNA clones (CASAR82A, -B, and -C) was strongly associated with resistance to C. coccodes [95]. This gene was mapped to the top of chromosome 5. C. annuum UENF 1381, in response to C. siamense, produced abundant amounts of antimicrobial peptides such as defensin, lipid transfer protein, and protease inhibitor [70]. The quantification of secondary metabolites produced during the interaction between the resistant C. annuum accessions GBUEL104 and C. siamense revealed that high concentrations of caffeic and chlorogenic acid were produced, and their differential expression depended on the fruit development stage and the time that had elapsed post-inoculation [55].

7. Conclusions

Anthracnose fruit rot disease is caused by a complex of Colletotrichum species. It causes significant yield losses and has become a constraint for Capsicum production. The ultimate means of achieving the sustainable control of anthracnose is to breed for anthracnose resistance. Worldwide screenings have mostly identified resistant accessions in C. baccatum and C. chinense. In this study, we summarized information on Capsicum accessions that have been tested and shown to be either resistant or susceptible to Colletotrichum spp. Generally, C. annuum lacks anthracnose resistance, but the introgression of resistance from resistant C. chinense and C. baccatum accessions has resulted in multiple breeding lines. A large number of genes and QTLs conferring anthracnose resistance that were anchored to the C. chinense and C. baccatum genomes were identified in various sources in the present study using an in silico mapping approach. Our results may be useful and informative for clarifying the locations of genes/QTLs from different sources for resistance to anthracnose rot disease in pepper, as well as for the introgression of resistance from donor accessions into elite cultivars.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy13051434/s1, Table S1: Published data on Capsicum accessions resistant to Colletotrichum species; Table S2: Published data on Capsicum accessions susceptible to Colletotrichum species; Table S3: Sequences from primer pairs, genes, proteins, or cDNA clones used in the in silico mapping of anthracnose resistance genes/QTLs [96,97,98,99,100,101,102,103].

Author Contributions

Conceptualization, Y.B. and R.E.V.; data curation, L.C. and M.C.v.d.M.; visualization and writing—original draft preparation, L.C.; writing—review and editing, L.C., M.C.v.d.M., Y.B. and R.E.V. All authors have read and agreed to the published version of the manuscript.

Funding

L.C. acknowledges financial support from the China Scholarship Council (201908140029).

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 13 01434 g001 550
Figure 1. Typical anthracnose symptoms after pinprick inoculation with C. siamense (previously known as C. gloeosporioides) on a red ripe fruit of chili.
Figure 1. Typical anthracnose symptoms after pinprick inoculation with C. siamense (previously known as C. gloeosporioides) on a red ripe fruit of chili.
Agronomy 13 01434 g001
Table
Table 2. Summary of identified sources of Capsicum accessions resistant to Colletotrichum species.
Table 2. Summary of identified sources of Capsicum accessions resistant to Colletotrichum species.
Colletotrichum Species aCapsicum Species b
C. annuumC. baccatumC. chacoenseC. chinenseC. frutescensCapsicum spp.
C. scovillei18464217-
C. capsici7622-1384
C. siamense3118-41-15
C. coccodes1---1-
C. brevisporum---15--
C. dematium7-----
C. truncatum9-----
Colletotrichum spp.18-----
Total160864901619
a C. scovillei (previously known as C. acutatum); C. siamense (previously known as C. gloeosporioides), and C. truncatum (previously known as C. capsici); resistance to multiple species (Colletotrichum spp.), including C. capsica (syn. C. truncatum), C. siamense, and C. scovillei was identified in 18 C. annuum accessions. b Capsicum spp. denotes that the Capsicum species was not mentioned in the corresponding reports; “-” no such report. Capsicum accessions resistant to Colletotrichum spp. were summarized from the following references: [13,16,25,26,28,30,31,35,36,39,41,44,45,46,47,48,49,51,52,53,54,55,56,59,61,62,63,64,65,66,67,68,69,70].
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Cui, L.; van den Munckhof, M.C.; Bai, Y.; Voorrips, R.E. Resistance to Anthracnose Rot Disease in Capsicum. Agronomy 2023, 13, 1434. https://doi.org/10.3390/agronomy13051434

AMA Style

Cui L, van den Munckhof MC, Bai Y, Voorrips RE. Resistance to Anthracnose Rot Disease in Capsicum. Agronomy. 2023; 13(5):1434. https://doi.org/10.3390/agronomy13051434

Chicago/Turabian Style

Cui, Lei, Michiel C. van den Munckhof, Yuling Bai, and Roeland E. Voorrips. 2023. "Resistance to Anthracnose Rot Disease in Capsicum" Agronomy 13, no. 5: 1434. https://doi.org/10.3390/agronomy13051434

APA Style

Cui, L., van den Munckhof, M. C., Bai, Y., & Voorrips, R. E. (2023). Resistance to Anthracnose Rot Disease in Capsicum. Agronomy, 13(5), 1434. https://doi.org/10.3390/agronomy13051434

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