Incidence and Severity of Aphid-transmitted Viruses and Horticultural Performance of Habanero Pepper (Capsicum chinense Jacq.) Breeding Lines in Benin

in HortScience
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Herbaud P.F. ZohoungbogboWorld Vegetable Center, West and Central Africa–Coastal and Humid Regions, IITA-Benin Campus, 08 BP 0932 Tri Postal Cotonou, Republic of Benin; and Laboratory of Genetics, Biotechnology and Seed Science, Faculty of Agronomic Sciences, University of Abomey-Calavi, BP 2549 Abomey-Calavi, Republic of Benin

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Enoch G. Achigan-DakoLaboratory of Genetics, Biotechnology and Seed Science, Faculty of Agronomic Sciences, University of Abomey-Calavi, BP 2549 Abomey-Calavi, Republic of Benin

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Judith HonfogaWorld Vegetable Center, West and Central Africa–Coastal and Humid Regions, IITA-Benin Campus, 08 BP 0932 Tri Postal Cotonou, Republic of Benin

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Shih-Wen LinWorld Vegetable Center, Shanhua, Tainan 74151, Taiwan

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Tsung-Han LinWorld Vegetable Center, Shanhua, Tainan 74151, Taiwan

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Yen-Wei WangWorld Vegetable Center, Shanhua, Tainan 74151, Taiwan

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Yuan-Li ChanWorld Vegetable Center, Shanhua, Tainan 74151, Taiwan

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Peter HansonWorld Vegetable Center, Shanhua, Tainan 74151, Taiwan

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Derek W. BarchengerWorld Vegetable Center, Shanhua, Tainan 74151, Taiwan

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Habanero (Capsicum chinense Jacq.) is widely grown and consumed in West and Central African countries, and viral diseases represent an important production challenge. Diagnosis of the viral species affecting habanero productivity in Benin is limited, and understanding this will enable more efficient host resistance breeding. During 2019 and 2020, we characterized the incidence and severity of the viral diseases infecting nine promising habanero breeding lines and one commercial hybrid check under open field conditions in Benin. The horticultural performance, including yield and yield component traits of the entries, was determined during the 2 years of the experiment. A randomized complete block design was used with three replications, each with 24 plants. Data were recorded on days to 50% flowering and 50% fruit maturity, yield and on the yield components of fruit weight (g), fruit length (cm), and fruit width (mm), as well as disease incidence and severity. In total, 35 leaf samples were collected for viral diagnosis among habanero breeding lines. We found that Pepper veinal mottle virus (PVMV; Potyvirus) was the overwhelmingly predominant virus in our trials, with an 80% incidence; however, we found frequent coinfection of PVMV with Cucumber mosaic virus (CMV, Cucumovirus), Polerovirus, and, to a lesser extent, Chili veinal mottle virus (ChiVMV; Potyvirus). The mean disease incidence across all entries was 60%. AVPP1932 and PBC 2010 had the lowest disease incidence (35% and 43%, respectively), whereas AVPP1929 had the highest (86%) disease incidence. The F1 hybrid check Afadja had the overall highest yield, with 30 t⋅ha−1, followed by AVPP1932, with 19 t⋅ha−1, both in 2019. There was a negative correlation between disease incidence and total yield (r = −0.44; P < 0.001), supporting previous studies indicating that viral diseases are major production constraints for habanero in West Africa. This study provides insight regarding the need to improve habanero for resistance to aphid-transmitted viruses and develop integrated pest management strategies to limit losses in Benin.

Abstract

Habanero (Capsicum chinense Jacq.) is widely grown and consumed in West and Central African countries, and viral diseases represent an important production challenge. Diagnosis of the viral species affecting habanero productivity in Benin is limited, and understanding this will enable more efficient host resistance breeding. During 2019 and 2020, we characterized the incidence and severity of the viral diseases infecting nine promising habanero breeding lines and one commercial hybrid check under open field conditions in Benin. The horticultural performance, including yield and yield component traits of the entries, was determined during the 2 years of the experiment. A randomized complete block design was used with three replications, each with 24 plants. Data were recorded on days to 50% flowering and 50% fruit maturity, yield and on the yield components of fruit weight (g), fruit length (cm), and fruit width (mm), as well as disease incidence and severity. In total, 35 leaf samples were collected for viral diagnosis among habanero breeding lines. We found that Pepper veinal mottle virus (PVMV; Potyvirus) was the overwhelmingly predominant virus in our trials, with an 80% incidence; however, we found frequent coinfection of PVMV with Cucumber mosaic virus (CMV, Cucumovirus), Polerovirus, and, to a lesser extent, Chili veinal mottle virus (ChiVMV; Potyvirus). The mean disease incidence across all entries was 60%. AVPP1932 and PBC 2010 had the lowest disease incidence (35% and 43%, respectively), whereas AVPP1929 had the highest (86%) disease incidence. The F1 hybrid check Afadja had the overall highest yield, with 30 t⋅ha−1, followed by AVPP1932, with 19 t⋅ha−1, both in 2019. There was a negative correlation between disease incidence and total yield (r = −0.44; P < 0.001), supporting previous studies indicating that viral diseases are major production constraints for habanero in West Africa. This study provides insight regarding the need to improve habanero for resistance to aphid-transmitted viruses and develop integrated pest management strategies to limit losses in Benin.

Chile pepper (Capsicum spp.) is an important crop grown worldwide that is widely used as a vegetable, spice, and pharmaceutical (Bosland and Votava, 2012). Chile pepper contains a wide range of bioactive compounds with functional properties with industrial interest. Among these compounds, capsaicinoids, which are secondary metabolites that elicit a spicy or hot flavor when consumed, are particularly important and contribute to the proliferation of chile pepper (Sanogo, 2003), phenolic compounds, carotenoids (provitamin A), and vitamins (C and E) (de Sá Mendes and de Andrade Gonçalves, 2020). Habaneros (C. chinense Jacq.) are good sources of lutein, cryptoxanthin, and beta-carotene, which are important carotenoids for human immune system function and eye health (Giuffrida et al., 2013; Guzman et al., 2021; Troconis-Torres et al., 2012).

In Africa, the productivity of the chile pepper is relatively low, with a mean yield of 15 t⋅ha−1, which is considerably lower than the mean yields in Europe and the Americas (40 t⋅ha−1 and 23 t⋅ha−1, respectively) (Food and Agriculture Organization of the United Nations, 2019). In West Africa, the low productivity of pepper is attributed to a number of biotic constraints (Idowu-Agida et al., 2010; Orobiyi et al., 2017). To limit losses associated with biotic stresses, West African chile pepper producers use various pesticides obtained from unlicensed dealers, and they usually do not follow the recommended doses and application frequencies (Doumbia and Kwadjo, 2009; Kanda et al., 2013). This sometimes leads to negative consequences for both the environment and the health of pesticide applicators and consumers. To limit pesticide abuse, it is imperative for farmers to adopt integrated pest and disease management strategies starting with the deployment of cultivars resistant or tolerant to the predominant diseases (Thresh, 2003).

In Benin, chile pepper is one of the most important cultivated and consumed crops, and it generates substantial income for smallholder farmers (Dossou et al., 2006). The cultivated varieties of chile pepper in Benin belong to three main species: C. annuum (L.), C. chinense, and C. frutescens (L.) (Akoègninou et al., 2006). The production of chile pepper in Benin faces many constraints, among which the unavailability of improved varieties, pests and diseases, and abiotic stresses are the most important (Orobiyi et al., 2013, 2017; Segnou et al., 2013). Afouda et al. (2013) found that viral diseases are among the major constraints limiting chile pepper production, especially in northern Benin. Cucumber mosaic virus (CMV; Cucumovirus), Pepper veinal mottle virus (PVMV; Potyvirus), Potato virus Y (PVY; Potyvirus), Tomato yellow leaf curl virus (TYLCV; Begomovirus), and members of Polerovirus have been identified in chile pepper fields in northern and southern Benin within the past 5 years (Afouda et al., 2017).

Strategies for managing viral diseases mostly focus on eradicating the vectors through intensive pesticide applications. However, the most effective means of managing viral diseases is by cultivating virus-resistant cultivars (Arogundade et al., 2012). Understanding which viruses infect chile pepper in West Africa and their relative importance is critical to establish a sound virus resistance breeding strategy. In this study, we evaluated the horticultural performance and the incidence and severity of viral diseases for promising habanero breeding lines to identify those lines adapted to Benin and West and Central Africa. The specific objectives were to 1) evaluate the horticultural performance of habanero pepper breeding lines, 2) evaluate the incidence and severity of viral diseases infecting habanero breeding lines, and 3) diagnose the viruses infecting habanero breeding lines.

Materials and Methods

Nine habanero pepper breeding lines were selected for evaluation based on their performance in multilocation trials in Benin and Taiwan (Zohoungbogbo et al., 2020) (Table 1). An F1 hybrid cultivar, Afadja, marketed in West Africa was provided by Rijk Zwaan Zaadteelt en Zaadhandel B.V. (De Lier, Netherlands), and used as a check in field trials. This study was conducted in the main rainy season from May to September in 2019 and 2020 at the World Vegetable Center at the West and Central Africa Regional Office in Abomey-Calavi in southern Benin (lat. 6.42°N; long. 2.33°E; elevation 51 m). Southern Benin is a relatively humid agroecological zone with two rainy seasons and a mean annual rainfall ranging from 1100 to 1400 mm/year (Yabi and Afouda, 2012). In both years, seeds of entries were sown in trays in a screenhouse in May and transplanted to the open field in June after plants reached the stage of four to six true leaves. Weather data during the experiment were recorded using a 3250 WatchDog Wireless Weather Station (Spectrum Technologies Inc., Aurora, IL) (Table 2).

Table 1.

Fruit color of the habanero (Capsicum chinense Jacq.) breeding lines and the hybrid check cultivar evaluated during 2 years (2019 and 2020) in Abomey-Calavi, Benin.

Table 1.
Table 2.

Summary weather data from April to September of 2019 and 2020 at Abomey-Calavi, Benin, recorded using a 3250 WatchDog Wireless Weather Station (Spectrum Technologies Inc., Aurora, IL).

Table 2.

The experiments followed a randomized complete block design with three replications, and each plot contained 24 plants. Plants were transplanted to two rows per bed with 70-cm centers and drip-irrigated. The within-row plant spacing was 50 cm. One week after transplanting, poultry manure was applied as sidedressing at a rate of 10 t⋅ha−1 and 2 weeks after transplanting, we applied a balanced fertilizer (N–P–K 15–15–15) at a rate of 200 kg⋅ha−1. Urea (46% N) and K2SO4 (50% K) fertilizers at a rate of 100 kg⋅ha−1 each were applied at 5 weeks after transplanting. The pesticides lambda-cyhalothrin 2.5 EC (Lambdacal; Arysta LifeScience, Paris, France) and mancozeb (Idefix; Savana Thonon-les-Bains, France) at a rate of 2 kg⋅ha−1 combined with metalaxyl (Acarius; Savana Thonon-les-Bains, France) at a rate of 300 mL⋅ha−1 were applied as needed to manage fungal diseases and mites based on regular scouting throughout the experiment. The experiments were managed according to the best management practices recommended by Berke et al. (2005). The fields were periodically hand-weeded throughout the growing season.

Days to 50% flowering and 50% fruit maturity, fruit length, fruit width, fruit weight, and fruit yield were recorded. Yield was determined by summing the total fruit weight from five harvests conducted 2 weeks apart. Total fruit yield (t⋅ha−1) was calculated by weighing all fruits harvested from each plot using a digital scale in kilograms and converting to t⋅ha−1 using the formula reported by Barchenger et al. (2018). Fruit weight was obtained from the average weight of five randomly selected fruits per plot. Fruit length and width were determined by measuring 10 randomly collected fully ripened fruits from the second and third harvests using calipers (Proster Trading Limited, London, England).

Individual pepper plants were evaluated for disease incidence and severity starting from the first appearance of symptoms in the field using a standardized 6-point scale modified from Sangsotkaew et al. (2019) and Fajinmi (2011), where 1 = no symptoms, 2 = very mild symptoms with slight yellowing only occurring near the petiole of young leaves, 3 = mild symptoms of slight yellowing of the entire area of young leaves, 4 = moderate symptoms of dark yellowing of young leaves and some old leaves, 5 = severe symptoms of dark yellowing of young and most of the old leaves, and 6 = very severe symptoms of complete plant yellowing, stunting, and lack of flower set. The occurrence of viral diseases resulted from natural pressure without artificial inoculation. The percent disease incidence in each plot was calculated by counting the number of diseased plants divided by the total number of pepper plants within the plot multiplied by 100. Disease severity was scored for each of the 24 plants in each plot two times during the trials (at the flowering and fructification stages). Severity data were collected during the second trial in May and Sept. 2020, and each plant in all plots of all entries was evaluated (at flowering and fruiting stages). The disease severity was estimated for each individual plant; then, the average disease severity was calculated for 24 plants in each plot using the formula used by Fajinmi (2011).

In 2019, 15 random plants with virus symptoms were sampled from the field. Similarly, in 2020, 20 leaf samples were collected: 10 from plants with typical symptoms of viral infection and 10 from asymptomatic plants. Leaf samples were collected and stored in zipper-locking plastic sampling bags that were labeled with an identifying tag number indicating the plot number, entry name, and collection date. After collection, samples were dried using silica gel for ≈48 h. All the samples were analyzed using the diagnostic techniques described by Barchenger et al. (2019).

For viral diagnosis, DNA was extracted from the collected samples and subjected to polymerase chain reaction amplification using universal Potyvirus primers (Gilbertson et al., 1991; Tsai et al., 2010). To test for the presence of CMV, PVY, Tomato mosaic virus (ToMV; Tobamovirus), Chili veinal mottle virus (ChiVMV; Potyvirus), PVMV, Pepper mild mottle virus (PMMoV; Tobamovirus), Tomato spotted wilt virus (TSWV; Tospovirus), Watermelon silver mottle virus (WMSMoV; Tospovirus), Pepper mottle virus (PMV; Tobamovirus), and nonspecific Potyvirus, crude sample homogenate (1:10 w/v) was subjected to a double- or triple-antibody sandwich enzyme-linked immunosorbent assay with appropriate proprietary antisera. To detect nonspecified Tospovirus and Polerovirus, total RNA was extracted and subjected to reverse-transcription polymerase chain reaction using universal primers of Tospovirus and Polerovirus, respectively.

Descriptive statistics including the mean and se were calculated for all quantitative traits (days to 50% flowering, days to maturity, yield, and yield components). Data were subjected to an analysis of variance using a linear mixed model with block, replication, year, and interaction effects considered as random effects and entry considered as a fixed effect. Tukey’s honestly significant difference was applied for means separation. Disease incidence data were transformed by the arcsin of the square root to normalize the data before applying the general linear models. Pearson’s correlation coefficient test was performed to determine associations among all traits evaluated. All analyses were performed using R software version 3.5.2 (R Core Team, 2018).

Results

The two-way interaction of entry × year significantly contributed to the variability observed for 50% flowering and 50% maturity. The average days to 50% flowering in our experiment was 49 d after transplanting. AVPP1932 was the earliest flowering entry in both years with 31 and 37 d after transplanting in 2019 and 2020, respectively. The latest flowering entry was AVPP1930 (62 d after transplanting) in 2019, followed by PBC 2010 in 2020 (59 d after transplanting) (Table 4). The average days to 50% fruit maturing in our experiment was 81 d after transplanting. AVPP1932 in 2019 was the earliest entry to reach 50% maturity at 47 d after transplanting. PBC 2010 in 2020 (104 d after transplanting) was the latest maturing entry (Table 4).

The two-way interaction of entry × year significantly contributed to the variability observed for total yield (Table 3). Although the main effect of year was not significant, generally, the performance in 2019 was numerically greater than in 2020. The average yield across entries in our experiment was 10.4 t⋅ha−1. The F1 hybrid check ‘Afadja’ had the highest yield (30 t⋅ha−1). With just more than 4 t⋅ha−1, PBC 2017 in 2020 was the lowest-yielding entry.

The two-way interaction of entry × year contributed to the variability for the yield component traits of fruit length and fruit weight, whereas the main effects of year and entry were significant for fruit width (Table 3). The average fruit weight among the entries in our experiment was 10.2 g. The average fruit length in our experiment was 42.7 cm. The hybrid check ‘Afadja’ in 2019 (26.0 g) had the greatest fruit weight, followed by AVPP1930 in 2020 (16.6 g), whereas PBC 2017 in 2019 (3.7 g) had the lowest fruit weight. The hybrid check ‘Afadja’ in 2020 had the greatest fruit length (8.2 cm), followed by AVPP1932 in 2020 (6.7 cm), whereas PBC 2010 in 2019 had the shortest fruit length (3.0 cm) (Table 4). Across all entries, the average fruit width was 3.3 cm in our experiment (Table 5). The widest fruit was found for AVPP1932 (4.1 cm) followed by the hybrid check ‘Afadja’ (3.9 cm), whereas PBC 2017 (2.3 cm) and AVPP1922 (2.7 cm) were found to have the narrowest fruit (Table 5).

Table 3.

Analysis of variance F-table with means squares for horticultural performance, yield, yield components, and virus incidence of the habanero (Capsicum chinense Jacq.) entries evaluated in Abomey-Calavi, Benin, in 2019 and 2020.

Table 3.
Table 4.

Days to 50% flowering and fruit maturity and yield and yield component means for the habanero (Capsicum chinense Jacq.) entries evaluated during the 2019 and 2020 seasons in Abomey-Calavi, Benin.

Table 4.
Table 5.

Viral disease incidence and fruit width of habanero (Capsicum chinense Jacq.) entries evaluated during the 2019 and 2020 seasons in Abomey-Calavi, Benin.

Table 5.

The main effects of entry and year significantly influenced viral disease incidence (P < 0.001) (Table 3). The overall average disease incidence was 60% across entries in our experiment. The highest affected entry was AVPP1929, with an incidence of 86%, and the lowest affected entry was AVPP1932, with an incidence of 35.8% (Table 5). The average viral disease incidences among the entries were 89% in 2020 and 30% in 2019.

Correlations were determined using the entry means across years because of the lack of interactive effects of year × entry for viral disease incidence. We observed that viral disease incidence was negatively correlated with total yield (r2 = −0.44; P = 0.0004). As expected, total yield was significantly positively correlated with fruit weight (r2 = 0.61; P < 0.001). Fruit width and fruit weight were significantly positively correlated (r2 = 0.65; P < 0.001) (Table 6).

Table 6.

Pearson correlation coefficients for disease incidence, yield, and yield components of the habanero (Capsicum chinense Jacq.) entries evaluated in Abomey-Calavi, Benin, in 2019 and 2020.

Table 6.

Disease severity was evaluated in 2020, and it was used to assess the extent to which each entry was affected by the virus. There was a significant difference among entries for viral disease severity (P = 0.022). Two entries, AVPP1932 and AVPP1925, developed very mild or moderate severity symptoms, with average viral disease severity scores of 2.89 and 2.95, respectively. Most of the entries had more severe disease severity, ranging from an average of 3 to 4 (AVPP1503, AVPP1930, PBC 2010, and PBC 2017) and from 4 to 5 (Afadja, AVPP1922, AVPP1923, and AVPP1929). The hybrid check, ‘Afadja’, had the highest disease severity rating (4.7) in the trial, followed by AVPP1923 (4.8) (Fig. 1).

Fig. 1.
Fig. 1.

Viral disease severity of the habanero (Capsicum chinense Jacq.) entries scored in 2020 using a standardized rating scale where 1 = no symptoms; 2 = very mild symptoms with slight yellowing only occurring near the petiole of young leaves; 3 = mild symptoms of slight yellowing of the entire area of young leaves; 4 = moderate symptoms of dark yellowing of young leaves and some old leaves; 5 = severe symptoms of dark yellowing of young and most of the old leaves; and 6 = very severe symptoms of complete plant yellowing, stunting, and lack of flower set.

Citation: HortScience 57, 5; 10.21273/HORTSCI16535-22

Samples were positive for CMV, ChiVMV, PVMV, WSMoV, and Polerovirus. Pepper veinal mottle virus was the overwhelmingly predominant virus in our trials, with an incidence of 80%; however, we found frequent coinfection of PVMV with CMV, Polerovirus, and, to a lesser extent, ChiVMV. None of the samples was found to be positive for Polerovirus alone in our experiment, and coinfection with members of the genus Potyvirus (27.3%) and CMV (4.5%) were common (Fig. 2). The coinfection of Polerovirus with CMV and Potyvirus occurred in 22.7% of the samples (Fig. 2). We found that 67% and 65% were positive for Polerovirus, 73% and 45% were positive for CMV, and 87% and 20% were positive for ChiVMV in 2019 and 2020, respectively. All viruses were present during both years of the experiment, with the exception of WSMoV (6%), which was only identified in 2019 (Table 7). The presence of Polerovirus and that of PVMV were similar for both years, but CMV and ChiVMV were more frequent in 2019 (Table 7).

Fig. 2.
Fig. 2.

Percentage of samples with single infection and coinfection of viruses among the habanero (Capsicum chinense Jacq.) entries evaluated in 2019 and 2020 in Abomey-Calavi, Benin.

Citation: HortScience 57, 5; 10.21273/HORTSCI16535-22

Table 7.

Percentage of leaf samples diagnosed with a viral infection that caused disease on the habanero (Capsicum chinense) entries evaluated during 2019 and 2020 in Abomey-Calavi, Benin.

Table 7.

Discussion

Breeding activities and other research focusing on habanero in West Africa and worldwide are largely lacking. Information about the adaptation and performance of habanero breeding lines across target environments enabling effective cultivar development is rare. Zohoungbogbo et al. (2020) evaluated a large panel of habanero entries and selected promising habanero breeding lines with a diversity of fruits shapes and colors observed at immature and mature stages. The current study expands on this preliminary research and further evaluates the promising breeding lines across 2 years, and it identified the predominant viral diseases infecting habanero in Benin.

Significant interactive effects of year and entry for days to flowering, days to maturity, yield, and the yield components of fruit length and fruit weight were observed in our study, but not for fruit width. Similarly, Soares et al. (2020) reported significant environment × entry interactive effects for yield and fruit length, but not fruit width, after evaluating advanced habanero breeding lines in Brazil. Traits such as fruit size have been reported to be highly heritable in chile pepper (Stommel and Griesbach, 2008), including members of C. chinense (Lozada et al., 2021). A strong genotype contribution to the variability of fruit weight, as compared with the environment, has also been reported for chile pepper (Barchenger et al., 2018). Conversely, traits such as the production of capsaicinoids have been found to be highly influenced by the growing environment (Jeeatid et al., 2018).

The habanero breeding lines evaluated in our study had a maximum yield of nearly 20 t⋅ha−1, and the hybrid check had a maximum yield of 30 t⋅ha−1, which are lower than the yields of habanero in Taiwan (Zohoungbogbo et al., 2020) and in Brazil (Soares et al., 2020), but similar to the yield of habaneros evaluated in Trinidad and Tobago (Ramjattan and Umaharan, 2021). The possible reasons for these differences include the difference in genotypes evaluated as well as the environment of the trials. Interestingly, the average values obtained for yield component traits of fruit length (range, 2.1–5.8 cm), fruit width (range, 2.3–4.1), and fruit weight (range, 3.7–16 g) are similar to those reported in Brazil, Mexico, and Trinidad and Tobago (Martinez et al., 2021; Meraz et al., 2018; Ramjattan and Umaharan, 2021; Ribeiro et al., 2015; Santana-Buzzy et al., 2016), but higher than those reported by Camposeco-Montejo et al. (2021) in Coahuila, Mexico.

The variability in horticultural performance of breeding lines enables genetic improvement and facilitates the development of cultivars adapted to new agroclimatic conditions or specific environments (Muñoz-Ramírez et al., 2020; Zewdie and Bosland, 2000). Most of the yield component traits of habanero are generally highly heritable (Manju and Sreelathakumary, 2006), although yield is heavily influenced by the environment. High diversity was observed in the breeding lines, and the highest performing breeding lines across years were AVPP1932, AVPP1503, and AVPP1922, which constitute a pool of candidate lines that could be exploited by breeding programs. As expected, the F1 hybrid check ‘Afadja’ generally performed better than all the inbred lines, indicating that the use of hybrid habanero cultivars in West Africa could result in increased production for farmers and supporting previous work involving hybrid habanero (Martinez et al., 2021; Muñoz-Ramírez et al., 2020; Yamazaki and Hosokawa, 2019). We found a significant negative correlation between virus incidence and yield, although the model did not explain a high percentage of the variable variation. The lower r2 could be because the effect of genotype on yield was highly significant as the main contributor to variability, thus limiting our ability to discern the individual environmental factors influencing yield. It is well known that viral infection can have a direct effect on yield (McKirdy et al., 2002). The predominant viral disease in our trial, PVMV, has been found to cause significant reductions in the yield of chile pepper (Fajinmi and Adebode, 2007); this is supported by our findings that AVPP1932 was among the most tolerant lines across the 2 years of experimentation and had the highest yield after the hybrid check.

Viral disease has a significant negative impact on chile pepper production in Africa and in West Africa. We found that CMV, ChiVMV, PVMV, PMMV, WSMoV, and Polerovirus were prevalent viruses in our field trials, thus supporting previous research identifying the major viruses of Capsicum spp. in West Africa as PVMV, ChiVMV, Tobacco etch virus (TEV; Potyvirus), Tobacco mosaic virus (TMV; Tobamovirus), Tomato mosaic virus (ToMV; Tobamovirus), PMMoV, Pepper leaf curl virus (PepLCV; Begomovirus), Tomato yellow leaf curl virus (TYLCV; Begomovirus), CMV, Alfalfa mosaic virus (AMV; Alfamovirus), TSWV, and Pepper vein yellows virus (PeVYV; Polerovirus) (Afouda et al., 2013, 2017; Arogundade et al., 2012, 2020; Seka et al., 2017; Tiendrébéogo et al., 2011; Tsai et al., 2010). We found that PVMV was the most commonly detected virus in the field trials both years. PVMV is a well-known chile pepper disease in Africa; in fact, PVMV was first found in chile pepper grown in Ghana more than 50 years ago (Brunt et al., 1978). Potyvirus is one of the larger groups of plant viruses and causes diseases in a wide range of plant species (Kenyon et al., 2014). All potyviruses are transmitted by one or more aphid species and can be transmitted mechanically and by grafting (Kenyon et al., 2014). PVMV has been widely reported in West Africa, including Benin, Burkina-Faso, Cote d’Ivoire, Ghana, Mali, Nigeria, Senegal, Sierra Leone, and Togo, and it is a serious problem for farmers (Afouda et al., 2013; Arogundade et al., 2012; Bolou Bi et al., 2018; Konaté and Traoré, 1999). Arogundade et al. (2012) reported that the high incidence of PVMV and/or CMV could be a result of numerous alternative host species surrounding the chile pepper fields.

No members of the genus Begomovirus were found in our study, contrary to previous studies (Afouda et al., 2013, 2017). The lack of begomoviruses in our experiment could have occurred because our trials were conducted during periods of low whitefly populations and low Begomovirus incidence. In Southern Benin, whiteflies, the vector of Begomovirus, are more commonly observed during the dry season (November–February). Another possible reason why begomoviruses were not identified is that pepper is typically less susceptible to TYLCV (and probably other monopartite begomoviruses), which has been identified in Benin (Afouda et al., 2013, 2017), compared with other begomoviruses such as Pepper leaf curl virus (Yule et al., 2019). However, the identification of several different aphid-transmitted viruses, mostly members of Potyvirus, supports previous findings (Afouda et al., 2013).

High coincidences of PVMV and Polerovirus were also detected. To the best of our knowledge, this is the first report of this coinfection occurring in Benin. Similar levels of mixed infection with Polerovirus have been observed in other parts of Africa (Buzkan et al., 2013; Waweru et al., 2021). The lack of Polerovirus infection occurring without coinfection of another or multiple viral species raises the question of whether the species is able to infect only if other viruses are already present. However, further work in this area is needed to clarify this. There was also a high coincidence of CMV and PVMV in the trials, which has been previously reported by Afouda et al. (2013). Interestingly, in our trials, we found that all the viruses detected, with the exception of WSMoV, were aphid-transmitted. Aphids are a common and highly threatening pest of Capsicum worldwide (Sun et al., 2020); although they do cause direct damage such as chlorosis, necrosis, wilting, stunting, and flower and fruit abortion, their role in vectoring plant viruses is more important (Frantz et al., 2004; Kenyon et al., 2014). Aphid control by farmers is currently performed using insecticides. However, the negative effects of excessive pesticide applications are well-known, leaving host resistance (Sun et al., 2018) in combination with integrated pest management strategies as the most viable option (Frantz et al., 2004). The breeding lines AVPP1932 and AVPP1925 were found to be field-tolerant to the predominant aphid-transmitted viruses and could be used in both breeding and integrated pest management schemes in the region to limit losses, although more screening is needed. The focus of breeding for Potyvirus resistance has been almost exclusively on C. annuum. The combination of the pvr6 gene, originating from ‘Perennial’, a member of C. annuum, and pvr21 or pvr22 alleles have been found to confer high levels of resistance to PVMV, whereas, individually, pvr6, pvr21, and pvr22 cannot confer resistance (Caranta et al., 1996). The introgression of a combination of multiple recessive resistance alleles certainly poses challenges to the development of resistant habanero cultivars, which is complicated by the high level of coinfection of multiple viral species observed in our trial. The best approach to developing resistant cultivars for West Africa is likely to build on the work established by Palloix et al. (2000) and work with a worldwide network of breeders and pathologists focusing on the viruses individually and in combination.

Conclusions

The diversity observed in the horticultural traits for the habanero breeding lines represents high genetic potential for further habanero breeding programs. The strong influence of growing environment on yield was expected, but there was some level of stability, with several lines performing well during both years of the experiment. The breeding lines AVPP1932, AVPP1922, and AVPP1503 could be used in breeding programs to potentially improve habanero production. The use of hybrid cultivars as compared with open-pollinated cultivars is a promising way to increase habanero yields. Predominantly aphid-transmitted viruses were identified in this study, but no begomoviruses were identified. Pepper veinal mottle virus was the main Potyvirus identified, with a high rate of coinfection with CMV and Polerovirus. The negative correlation between yield and viral disease incidence supports the use of host resistance. Deploying cultivars resistant to aphid-transmitted viruses, specifically PVMV, managing aphids, and the development and adoption of hybrid cultivars are important to improving habanero production in Benin and West Africa.

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Contributor Notes

Funding for this research was provided by UK aid from the UK government through the project “Developing and delivering agricultural technologies and knowledge to reduce poverty and hunger, and support adaptation to climate change” and by long-term strategic donors to the World Vegetable Center: Taiwan, United States Agency for International Development (USAID), Australian Centre for International Agricultural Research (ACIAR), Germany, Thailand, Philippines, Korea, and Japan.

Data available in a publicly accessible repository. All data collected during this experiment were deposited in the World Vegetable Center repository, HARVEST (https://worldveg.org/harvest) and are available to the public.

We appreciate the excellent work of the field technicians involved in trials management and data collection. We are thankful to Azoma Komla for the help in the trial implementation and data collection.

D.W.B. is the corresponding author. E-mail: derek.barchenger@worldveg.org.

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    Fig. 1.

    Viral disease severity of the habanero (Capsicum chinense Jacq.) entries scored in 2020 using a standardized rating scale where 1 = no symptoms; 2 = very mild symptoms with slight yellowing only occurring near the petiole of young leaves; 3 = mild symptoms of slight yellowing of the entire area of young leaves; 4 = moderate symptoms of dark yellowing of young leaves and some old leaves; 5 = severe symptoms of dark yellowing of young and most of the old leaves; and 6 = very severe symptoms of complete plant yellowing, stunting, and lack of flower set.

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    Fig. 2.

    Percentage of samples with single infection and coinfection of viruses among the habanero (Capsicum chinense Jacq.) entries evaluated in 2019 and 2020 in Abomey-Calavi, Benin.

  • Afouda, L., Kone, D., Zinsou, V., Dossou, L., Kenyon, L., Winter, S. & Knierim, D. 2017 Virus surveys of Capsicum spp. in the Republic of Benin reveal the prevalence of Pepper vein yellows virus and the identification of a previously uncharacterised Polerovirus species Arch. Virol. 162 1599 1607 https://doi.org/10.1007/s00705-017-3274-8

    • Search Google Scholar
    • Export Citation
  • Afouda, L.A., Kotchofa, R., Sare, R., Zinsou, V. & Winter, S. 2013 Occurrence and distribution of viruses infecting tomato and pepper in Alibori in northern Benin Phytoparasitica 41 271 276 https://doi.org/10.1007/s12600-013-0287-z

    • Search Google Scholar
    • Export Citation
  • Akoègninou, A., Van der Burg, W.J. & Maesen, L.J.G.V.d. 2006 Flore analytique du Bénin No. 06.2 Backhuys Publishers (Wageningen Agricultural University papers 06.2) (in French)

    • Search Google Scholar
    • Export Citation
  • Arogundade, O., Ajose, T., Osijo, I., Onyeanusi, H., Matthew, J. & Aliyu, T.H. 2020 Management of viruses and viral diseases of pepper (Capsicum spp.) in Africa 73 77 Dekebo, A. Capsicum. IntechOpen Limited London, UK https://dx.doi.org/10.5772/Intechopen.87455

    • Search Google Scholar
    • Export Citation
  • Arogundade, O., Balogun, O.S. & Kareem, K.T. 2012 Occurrence and distribution of Pepper veinal mottle virus and Cucumber mosaic virus in pepper in Ibadan, Nigeria Virol. J. 9 1 4 https://doi.org/10.1186/1743-422X-9-79

    • Search Google Scholar
    • Export Citation
  • Barchenger, D.W., Clark, R.A., Gniffke, P.A., Ledesma, D.R., Lin, S.-W., Hanson, P. & Kumar, S. 2018 Stability of yield and yield components of pepper (Capsicum annuum), and evaluation of publicly available predictive meteorological data in East and Southeast Asia HortScience 53 1776 1783 https://doi.org/10.21273/HORTSCI13581-18

    • Search Google Scholar
    • Export Citation
  • Barchenger, D.W., Yule, S., Jeeatid, N., Lin, S.-W., Wang, Y.-W., Lin, T.-H., Chan, Y.-L. & Kenyon, L. 2019 A novel source of resistance to Pepper yellow leaf curl Thailand virus (PepYLCThV) (Begomovirus) in chile pepper HortScience 54 2146 2149 https://doi.org/10.21273/HORTSCI14484-19

    • Search Google Scholar
    • Export Citation
  • Berke, T., Black, L.L., Talekar, N.S., Wang, J.F., Gniffke, P., Green, S.K., Wang, T.C. & Morris, R. 2005 Suggested cultural practices for chili pepper AVRDC Publ. 05 620

    • Search Google Scholar
    • Export Citation
  • Bolou Bi, B., Moury, B., Abo, K., Sorho, F., Cherif, M., Girardot, G., Kouassi, N. & Kone, D. 2018 Survey of viruses infecting open-field pepper crops in Côte d’Ivoire and diversity of Pepper veinal mottle virus and Cucumber mosaic virus Plant Pathol. 67 1416 1425 https://doi.org/10.1111/ppa.12849

    • Search Google Scholar
    • Export Citation
  • Bosland, P.W. & Votava, E.J. 2012 Peppers: Vegetable and spice capsicums 2nd ed. CAB International Wallingford, UK

  • Brunt, A., Kenten, R. & Phillips, S. 1978 Symptomatologically distinct strains of Pepper veinal mottle virus from four West African solanaceous crops Ann. Appl. Biol. 88 115 119 https://doi.org/10.1111/j.1744-7348.1978.tb00685.x

    • Search Google Scholar
    • Export Citation
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