Open-access Searching for common bean genotypes resistant to Acanthoscelides obtectus, a primary pest species of stored beans

ABSTRACT

Resistant genotypes are a valuable tool in integrated pest management programs of insect pests of stored grains. Here, we screened 90 Brazilian common bean genotypes to select promising sources of resistance to Acanthoscelides obtectus. Thus, bean samples were infested with newly emerged insects, and the number of eggs, emerged insects, developmental time, and larval viability were assessed in a no-choice test. Genotypes IPR Garça, CHIR 13, IAC Harmonia, CHIR 20, IAC Boreal, and CHIP 312 showed low oviposition. Genotypes IPR Quero-Quero, BRS Notável, CHIC 61 - Cariocão, BRS Ametista, IPR Uirapuru, IAC Imperador, Avaluna, CHP 04-241A-212 - Guapo B. × Uirapuru, CHIB 06, SCS 206 - Potência, CHC 01-175-1 - Campeiro × IAC Tibatã, CHP 01-182-48 - Uirapuru × Campeiro, UEM 266, CHC 04-233-2 - Siriri × Horizonte, CHV 17-64, SCS 205 - Riqueza, CHP 01-238-80 - MN 13337, SM 1510 - preto, BRS Radiante, CHIB 18, CHIR 14, CAV 17 EFM 008, CHIR 04, IPR Campos Gerais, CHV 05-268-02, LP 13-624 - preto, Linhagem 110 - IAC, CHP 01-182-12 - Uirapuru × Campeiro, LP 13-84 - carioca, BRS Esteio, CHV 17-635, CHB 15-518, Arcelina 1, IPR Tuiuiu, SCS 204 - Predileto, TB - 17-02, BRS Estilo, SM 0511 - cavalo preto, Pérola, IPR Tangará, and CNFRj - 15411 reduced oviposition, the number of emerged adults, and larval viability, suggesting antixenosis and/or antibiosis. Thus, these genotypes are promising sources of resistance factors and can be used in breeding programs to obtain lines of common beans resistant to A. obtectus.

Key words  Phaseolus vulgaris ; bean weevil; host plant resistance; antixenosis; antibiosis

INTRODUCTION

The common bean, Phaseolus vulgaris L. (Fabales: Fabaceae), is a major source of proteins, carbohydrates, vitamins, and minerals (Mendoza and Sánchez 2017). This legume is an important component of human diets both in developing and underdeveloped countries, contributing significantly to the reduction of malnutrition in rural and urban areas, while increasing food security (Nassary et al. 2020, Nadeem et al. 2021, Nchanji and Lutomia 2021). The common bean also has other beneficial biological activities, such as a powerful antioxidant activity due to the high content of polyphenols in its grains (Messina 2014, Celmeli et al. 2018).

Despite its socioeconomic importance, significant amounts of common bean are lost during storage in warehouses, mainly due to the incidence of insect pests (Gonçalves et al. 2015, Adler et al. 2022), because of climatic conditions in tropical regions that favor the development of this biota, in addition to the unsatisfactory storage conditions (Ribeiro et al. 2013). One of the most serious pests of stored beans worldwide is the bean weevil Acanthoscelides obtectus (Say, 1831) (Coleoptera: Chrysomelidae: Bruchinae) (Paul et al. 2009, Thakur 2012, Naroz et al. 2019). The infestation by this bruchid can occur during bean storage or even in the field (Guzzo et al. 2018). In most cases, larvae are carried to warehouses inside the grains infested in the field and, as they develop, the larvae damage the grains mainly by feeding on their internal content. Later, severe losses are detected as consequence of adult emergence. In some cases, the grains are completely destroyed, affecting seed germination and compromising the commercial value of beans because of grain weight reduction and interference on bromatological characteristics (Ishimoto and Chrispeels 1996, Baldin et al. 2017, Mutungi et al. 2020). Moreover, insect-related damage in warehouses, along with inadequate storage devices, compromises food security mainly for smallholder farmers that use the common bean as part of family diet (Endshaw and Hiruy 2020).

The chemical control by synthetic insecticides is the most used method to A. obtectus management in warehouses, in addition to curative fumigation (phosphine) and preventative spray of insecticides, mainly pyrethroids and organophosphates (Agrofit 2023). Nevertheless, insecticide overuse and the limited number of products available with different mode of action compromise the strategies of insecticide resistance management, thus increasing the incidence of resistant insect populations (Guedes et al. 2009). Furthermore, there is growing social concern regarding the possible accumulation of chemical residues on treated grains, especially when insecticide applications occur near the time to consume the product (Kljajić et al. 2023). This scenario requires the search for alternative control methods or complementary strategies for integrated pest management programs, such as the development of resistant genotypes (Baldin et al. 2019). Resistant genotypes provide desirable characteristics, such as specificity to the target organism, harmony with the environment, action on successive insect generations, and compatibility with other management tactics used in integrated pest management (Smith and Clement 2012, Baldin et al. 2019).

In the search for resistance sources in P. vulgaris genotypes, some studies have detected promising resistant genotypes to A. obtectus, indicating different levels of antixenosis and/or antibiosis (Schoonhoven et al. 1983, Cardona et al. 1989, Velten et al. 2007, Zaugg et al. 2012, Guzzo et al. 2015, Baldin et al. 2017). For example, the QUES wild accession showed the lowest A. obtectus emergence rates, a smaller number of emerged adults, and longer developmental times (Zaugg et al. 2012). In RAZ lines (arcelin-containing beans), the time until adult emergence was significantly prolonged when compared to susceptible standards and resulted in lower body weight of females (Velten et al. 2007). On the other hand, Cardona et al. (1989) verified that population growth rates of A. obtectus were negatively affected by G12952 bean accession. The authors also reported prolonged life cycles, a smaller number of emerged adults, high mortality of late first instars, and reduced female fecundity. In the laboratory, Baldin et al. (2017) identified the genotypes Arc.1, Arc.2, Arc.1S, Arc.5S as resistant to A. obtectus, expressing antibiosis by prolonged life cycle and decreased emergence rates. The authors also demonstrated that morphological factors, such as pod surface (chemicals, trichomes, texture) and wall properties (lignified, thickened), are related to antixenosis type resistance observed in Arc.1 and Arc.1S genotypes, in greenhouse tests.

Most studies available, however, were carried out more than a decade ago or investigated a germplasm with restricted genetic variability (some are even currently unavailable), which hinders the use of these sources in breeding programs aiming to obtain resistant genotypes to the bean weevil. In this context, we evaluated the expression of resistance to A. obtectus in 90 Brazilian genotypes of P. vulgaris, some were evaluated against stored insect pests for the first time. The results of this comprehensive screening are useful for breeding programs to develop lines resistant to the bean weevil.

MATERIAL AND METHODS

Insects

The bean weevils used in the bioassays were obtained from a stock rearing kept in a climatized chamber (25 ± 2°C, relative humidity = 70 ± 10%, and photoperiod of 12:12 h L:D). For colony maintenance, clear glass flasks (800 mL) were used, closed at the top with organdy fabric, allowing internal aeration. Each flask was filled with 300 g of bean grains cv. Bolinha and approximately 100 unsexed adult insects. The grains in the flasks were sieved every 28 days, and the newly emerging adults were used to infest new flasks or in the bioassays proposed.

Bean genotypes

The genotypes studied were obtained from the germplasm banks of the Agronomic Institute of Campinas (IAC) and the Agricultural Research and Rural Extension Company of Santa Catarina. Their respective genealogies, origin, and additional information are described in Table 1. In the bioassays, genotype IAC UNA was included as a susceptible standard (Guzzo et al. 2015, Eduardo et al. 2016).

Table 1
Common bean genotypes evaluated for resistance to Acanthoscelides obtectus and their respective genealogy.

Bioassays

Transparent acrylic containers of 50 mL (experimental units) with lids (5 cm height × 3 cm diameter) were used to accommodate 5 g of bean grains from each genotype tested. The grains were weighed on an analytical balance at the accuracy of 0.001 g. Afterward, 10 unsexed adults with ages between 0–48 h, randomly collected from the stock rearing, were released into each container for oviposition for seven days (Baldin and Lara 2008). The difference between male and female is observed from the inclination of the pygidium, vertical in males and oblique in females (Athié and Paula 2002), and the sex ratio of the species is 1:1 of male and female (Howe and Currie 1964). Thus, unsexed adults were used in the initial screening due to the large number of genotypes tested and the difficulty of sexing.

After preparation and insect infestation, the experimental units were stored in a biochemical oxygen demand chamber (25 ± 2°C, relative humidity = 70 ± 10%, and photoperiod of 12:12 h L:D). After seven days, adults were removed, and the number of total eggs, viable eggs, and non-viable eggs were counted at 21 days after infestation with the aid of a stereoscopic microscope (40x magnifications). The grains of each plot were deposited in Petri dishes (90 × 15 mm) covered with black cardboard to facilitate visualization of the eggs deposited between the grains. Viable eggs had a larval exit hole, while non-viable eggs were intact with a hyaline coloration aspect (Ribeiro-Costa et al. 2007).

Twenty-eight days after the initial infestation, the number of emerged insects and the developmental time (egg-adult) were also determined by sieving the grains of each container through an appropriate mesh and by counting the number of insects emerging per day and per genotype, until there were no more emergences for five consecutive days. The weighted mean calculated by the Eq. 1 was used to determine the egg-to-adult developmental time.

Σ x f / Σ x (1)

where: x: the number of adults emerging in that day; f: the number of emergence days (Costa and Boiça Júnior 2004).

Larval viability was calculated based on the number of viable eggs and the number of emergences per genotype. The experimental design was completely randomized with four repetitions per genotype. Each container with 5 g of grains and 10 insects was considered as a repetition.

Statistical analysis

For the data analysis, we first verified the normality of residues with the Shapiro-Wilk test (Shapiro and Wilk 1965), as well as the homogeneity of variances with the Levene test (Levene 1960). When assumptions were satisfied, the data were submitted to the analysis of variance, and the means were compared by the Scott-Knott test (p < 0.05). The statistical software Statistical Analysis System (version 9.2) was used for the analyses.

The multivariate cluster analysis was performed to verify the grouping of the genotypes studied using the following variables: larval viability (%), number of emerged adults, developmental time, and total number of eggs. The mean Euclidean distance, as a measure of dissimilarity, and the average method as a clustering strategy were used because they had the highest co-optic correlation (Manly 2004). The cut-off was established considering half of the maximum adjusted Euclidian distance (Fávero and Belfiore 2017).

RESULTS

There was significant variation in oviposition of A. obtectus between the different bean genotypes studied (Table 2). Regarding the total number of eggs, genotypes BRS Notável, IPR Quero-Quero, BRS Ametista, IPR Uirapuru, Linhagem 110 - IAC, Avaluna, IAC Imperador, CHIB 06, SCS 206 - Potência, CHIC 61 - Cariocão, IPR Tangará, CHIR 13, CHP 04-241A-212 - Guapo B. × Uirapuru, Pérola, CNFRj - 15411 - Rajado, CHC 04-233-2 - Siriri × Horizonte, CHP 01-182-48 - Uirapuru × Campeiro, CHC 01-175-2 Campeiro × Tiba F11, UEM 266, CHC 01-175-1 - Campeiro × IAC Tibatã, SCS 204 - Predileto, LP 13-84 - Carioca, TB - 17-02, IPR Garça, BRS Esteio, CHIP 283, BRS Estilo, Arcelin 1, SM 0511 - Cavalo Preto, CHP 01-182-12 - Uirapuru × Campeiro, IPR Tuiuiu, CHIP 295, CHV 17-635, IAC Boreal, CHIR 20, CHIP 315, CHB 15-518, CAV 17 EFM 0007, CHC 00-101-10 Pérola × IAC F8, CAV 17 EFM 008, CHV 17-641, CHIM 15, CHIR 14, Arcelin 3, and CHIB 11 were the less oviposited (between 15.75 and 75.50 eggs/sample; Table 2). These genotypes had lower oviposition compared to genotype IAC UNA, used as a susceptible standard, and were chosen based on the studies of Guzzo et al. (2015) and Eduardo et al. (2016) (Table 2). The same genotypes with the smallest means of total eggs also had the smallest means of viable eggs (Table 2); however, there was no significant difference between all genotypes tested in terms of the number of unviable eggs (Table 2).

Table 2
Means (± standard error) of number of total eggs, viable eggs, unviable eggs, emerged adults, larval viability (%) and developmental time (days) of Acanthoscelides obtectus in different common bean genotypes1 1 Means within the columns followed by the same letters are not significantly different by the Skott-Knott test (p < 0.05). .

Genotypes BRS Notável, IPR Quero-Quero, BRS Ametista, IPR Uirapuru, Linhagem 110 - IAC, Avaluna, IAC Imperador, CHIB 06, SCS 206 - Potência, CHIC 61 - Cariocão, IPR Tangará, CHP 04-241A-212 - Guapo B. × Uirapuru, Pérola, CNFRj - 15411 - Rajado, CHC 04-233-2 - Siriri × Horizonte, CHP 01-182-48 - Uirapuru × Campeiro, CHC 01-175-2 Campeiro × Tiba F11, UEM 266, CHC 01-175-1 - Campeiro × IAC Tibatã, SCS 204 - Predileto, LP 13-84 - Carioca, TB -17-02, BRS Esteio, BRS Estilo, Arcelin 1, SM 0511 - Cavalo Preto, CHP 01-182-12 - Uirapuru × Campeiro, IPR Tuiuiu, IAC Harmonia, CHV 17-635, CHB 15-518, CAV 17 EFM 008, CHIR 04, CHIB 18, CHV 17-641, CHIM 15, CHIR 14, SCS 205 - Riqueza, Arcelina 3, BRS Radiante, SM 1510 - Preto, CHP 01-238-80 - MN 13337, CHIB 11, IPR Campos Gerais, LP 13-624 - Preto, CHV 05-268-02, CHP 05-282-04 - Campeiro × Agudo, CHC 01-167-1-03, TB - 17-03, CHIB 07, CAV 17 EFM 0006, BRS Esplendor, and BRS Campeiro showed a significant reduction in the number of emerged adults (between 2 and 28.25 adults/sample). The remaining genotypes showed high emergence in comparison to most susceptible genotypes, as well as a similar behavior to the genotype adopted as a susceptible standard (IAC UNA) (Table 2).

The same genotypes with lower averages of emerged adults showed low percentage of larval viability (%), in addition to genotypes IPR Siri and excluding IAC Harmonia (Table 2). Genotypes IPR Uirapuru, CHIB 06, CHIC 61 - Cariocão, IPR Tangará, CHIR 13, CNFRj - 15411 - Rajado, CHP 01-182-48 - Uirapuru × Campeiro, CHC 01-175-1 - Campeiro × IAC Tibatã, SCS 204 - Predileto, LP 13-84 - Carioca, BRS Estilo, Arcelin 1, IPR Tuiuiu, CHV 17-635, CHB 15-518, CHIP 305, CHIB 18, CHV 17-641, CHIR 14, Arcelin 3, SM 1510 - Preto, CHIP 347, IAC Diplomata, CHIB 12, CHIP 175, TB - 17-03, ANFc09, CHB 15-519, CHIB 07, CAV 17 EFM 0006, IPR Siriri, BRS Esplendor, and BRS Campeiro showed the largest means for the developmental time (egg-to-adult period) (between 34.82 and 39.25 days), differing from the other genotypes tested, including the IAC UNA susceptible standard (Table 2).

The multivariate cluster analysis resulted in five groups using the variables of larval viability, number of adults emerged, developmental time, and total number of eggs, as well as half of maximum Euclidean distance adjusted as a cut-off point (Fávero and Belfiore 2017) (Fig. 1).

Figure 1
Dendrogram obtained from the cluster analysis based on similarity of biological parameters (larval viability, number of emerged adults, developmental time, and total number of eggs) of Acanthoscelides obtectus on common bean (Phaseolus vulgaris L., Fabaceae) genotypes. The mean Euclidean distance was used as a measure of dissimilarity and the average method as a clustering strategy [the cut-off was established considering half of maximum adjusted Euclidian distance (41); (dashed line)].

Group I was the most distinct and was composed only of genotype CHC 97-29-07 - Sel PL. Ind. V2, which exhibited the largest means in all parameters evaluated and behaved as the most susceptible genotype. Group II was the most inclusive, with 41 genotypes (IPR Quero-Quero, BRS Notável, CHIC 61 - Cariocão, BRS Ametista, IPR Uirapuru, IAC Imperador, Avaluna, CHP 04-241A-212 - Guapo B. × Uirapuru, CHIB 06, SCS 206 - Potência, CHC 01-175-1 - Campeiro × IAC Tibatã, CHP 01-182-48 - Uirapuru × Campeiro, UEM 266, CHC 04-233-2 - Siriri × Horizonte, CHV 17-64, SCS 205 - Riqueza, CHP 01-238-80 - MN 13337, SM 1510 - Preto, BRS Radiante, CHIB 18, CHIR 14, CAV 17 EFM 008, CHIR 04, IPR Campos Gerais, CHV 05-268-02, LP 13-624 - Preto, Linhagem 110 - IAC, CHP 01-182-12 - Uirapuru × Campeiro, LP 13-84 - Carioca, BRS Esteio, CHV 17-635, CHB 15-518, Arcelina 1, IPR Tuiuiu, SCS 204 - Predileto, TB - 17-02, BRS Estilo, SM 0511 - Cavalo Preto, Pérola, IPR Tangará and CNFRj - 15411), congregating the genotypes with the lowest oviposition and smallest number of emerged insects and consequently lower means of larval viability.

On the other hand, group III was represented by genotypes CHIP 282, FAP-F3-2 SEL - IAC, CHB 15-519, IAC Jabola, CAV 17 EFM 0006, IPR Siriri, BRS Campeiro, BRS Esplendor, CHIB 07, TB - 17-03, CHP 05-282-04 - Campeiro × Agudo and CHC 01-167-1-03, which exhibited a larger number of eggs. Group IV congregated genotypes IPR Garça, CHIR 13, IAC Harmonia, CHIR 20, IAC Boreal and CHIP 312, grouping the genotypes with the shortest developmental time and lowest oviposition. Conversely, these materials showed larger means of emerged adults and larval viability (%).

Finally, group V was composed by genotypes CHIP 297, CHIP 346, IAC Alvorada, CHP 04-239-S2, IAC Formoso, ANFc09, CHIN 19, CHIB 12, CHIM 03, CHIR 05, IAC UNA (susceptible standard), CHIP 334, CHC 04230-2, CHIP 175, CNFRs - 15558 - Rosinha, CHIP 347, LEC 04-16, CHC 98-42-IAC Eté × FEB 189 F9, IAC Diplomata, CAV 17 EFM 0007, CHIP 315, CHIP 295, CHIB 11, CHP 01-238-10, CHIM 15, Arcelin 3, CHC 01-175-2 Campeiro × Tiba F11, CHIP 283, CHC 00-101-10 Pérola × IAC F8, and CHIP 305 congregated genotypes with the highest oviposition rates, the largest number of emerged adults, and the highest larval viability. In contrast, these genotypes showed the lowest developmental time.

DISCUSSION

Our comprehensive screening with a diversified group of Brazilian bean genotypes showed a large behavioral variation in terms of resistance to A. obtectus. Thus, the most promising genotypes should be used in breeding programs to obtain common bean lines resistant to A. obtectus, a bruchid pest species of importance worldwide. In addition, these genotypes should preferably be cultivated by small farmers in regions where this pest species is considered the most important in the post-harvest period.

Our results demonstrate that the less oviposited genotypes indicate resistance expression of antixenosis in a no-choice test (Baldin et al. 2019). The choice for oviposition sites by pests of stored grains can be influenced by several physical and morphological causes, as reported by Azizoglu (2018), who indicated a negative correlation between tegument hardness and larval penetration. The authors reported that the common bean genotype Akdağ with the highest thickness tegument had the lowest infestation rate by A. obtectus. Gbaye and Holloway (2011) stated that seed colors are directly related to colonization of Callosobruchus maculatus (F.) (Coleoptera: Chrysomelidae: Bruchinae), while Nazzi et al. (2008) observed that semiochemicals released by P. vulgaris seeds directly influenced the host-related behavior of A. obtectus.

Host attraction of weevils to dry beans guided by olfactory cues has been reported for a long time (Larson and Fisher 1938). The bean weevil A. obtectus exhibits a different fecundity process from other bruchids. The species oviposition peak occurs on the fourth or fifth day after emergence (Parsons and Credland 2003), unlike other species that have their peak oviposition rate on the first or second day after emergence, such as C. maculatus and Callosobruchus chinensis (L.) (Coleoptera: Chrysomelidae: Bruchinae) (Avidov et al. 1965; Dick and Credland 1984). This may be partially attributed to the requirement of a host stimulant for maximal oogenesis and oviposition in some A. obtectus populations.

The considerable number of viable eggs considering the total number of eggs indicated that the larvae penetrated the grain. The percentage means of larval viability were smaller, possibly because of the presence of some compound that plays an antibiotic role, showing that many insects did not reach the adult stage due to the ingestion of some substances (allelochemicals). The analysis of intake per insect and the weight of emerged adults are important parameters to discriminate the types of resistance (Baldin et al. 2019) and should be considered in future tests with promising resistance genotypes to A. obtectus.

Some genotypes have a combination of chemical and morphological factors that negatively affect insect behavior or development, hindering the process to isolate causes of antibiosis and antixenosis (Smith and Clement 2012). Therefore, characterization of resistance types in bean genotypes should be subjected to further investigations. However, the smaller number of emerged adults, the decrease of larval viability, and the delayed egg-to-adult developmental time of the genotypes tested may be an indicative of antibiosis resistance (Baldin et al. 2019). These results are possibly related to toxic compounds that delay the development of immature stages of insect pests, such as antibiotics, alkaloids, terpenes, cyanogenic glycosides, and proteins (Gepts 1999, Paes et al. 2000, Sakthivelkumar et al. 2013).

The main proteins associated to bean genotypes resistant to bruchids are lectins, α-amylase inhibitors, proteinase inhibitors, inactivating-protein ribosomes, protein reserves (vicilin) of modified proteins, proteins involved in lipid transport, glucanases, arcelins, and chitinases (Chrispeels and Raikhel 1991, Kasahara et al. 1996, Grossi de Sá and Chrispeels 1997, Franco et al. 1999, Carlini and Grossi de Sá 2002, Baldin and Pereira 2010; Zaugg et al. 2012). These resistance factors can affect nutrient assimilation, delaying insect development or causing its death (Amorim et al. 2008). Thus, further studies should be conducted to assess physical, morphological, and chemical factors associated to resistant bean genotypes.

Studies that mapped common bean resistance genes to weevils found that the expression level of the Phvul.006G003700 gene in resistant cultivars was much higher compared to genotypes susceptible to bruchids, possibly related to the expression of increased production of α-amylase inhibitors (Li et al. 2022). This enzyme in the saliva and gut of insects and proteinase inhibitors, when linked to digestive enzymes, may be responsible for decreasing insect feeding, producing an anti-insect effect (Boyd et al. 2002). Other authors also confirmed that α-amylase inhibitors are closely related to resistance expression to A. obtectus and other bruchids (Basi et al. 1993, Franco et al. 2000, Lüthi et al. 2013).

Arcelin is a protein toxic to several insects, including A. obtectus and Zabrotes subfasciatus (Mazzonetto and Vendramim 2002, Baldin and Pereira 2010, Baldin et al. 2017, Tigist et al. 2021). Currently, eight variants of arcelin have been identified in wild beans with different resistance levels to bruchids (Osborn et al. 1986, Lioi and Bollini 1989, Cardona et al. 1990, Santino et al. 1991, Acosta-Gallegos et al. 1998, Zaugg et al. 2012). However, some authors proposed that arcelin has little effect on A. obtectus, compared to other bruchids (Hartweck et al. 1997, Guzzo et al. 2015). In the present study, Arcelin 1 was associated to genotypes with lower oviposition, smaller number of emerged insects, and consequently smaller means of larval viability (Fig. 1), suggesting the action of the protein in bean resistance to this bruchid (Smith and Clement 2012).

Baldin et al. (2017) used the same method and reported that genotypes Arcelin 1, Arcelin 2, Arcelin 1S, Arcelin 5S, and Arcelin 3S showed antibiosis resistance against A. obtectus, corroborating with the results of the present study. Conversely, in the present study genotype Arcelin 3 was grouped with genotypes with the highest oviposition, the largest number of emerged insects, and the highest larval viability (Fig. 1), which could be related to the different resistance levels of arcelin variants or associated to species specific plant resistance to insects (Lara 1991, Smith 2005).

Exposure to plant proteinase inhibitors and α-amylase inhibitors may have negative and positive effects on human physiology and well-being (Clemente et al. 2010, Oliás et al. 2019). Some phytochemicals of legume and cereal, such as α-amylase and α-glucosidase, represent a potential medicine for antidiabetic and overweight treatments due to slower carbohydrate absorption (Payan 2004, Ch’ng et al. 2019). On the other hand, some plant-derived compounds, naturally present in legume and cereal composition, may affect the digestive processes in the human gastrointestinal system and make plant protein less bioaccessible in the human organism (Tomé 2013). Li et al. (2021) reported that proteases inhibitors can be divided into six different classes (knottin-like, Kunitz, thaumatin-like, γ-thionin-like, cereal, and lectin-like). According to these authors, the first three classes affect only amylases of insects and can be therefore used as pest control methods. Therefore, a careful assessment of the antibiotic compounds in these genotypes is needed to ensure food security to many people.

Previous studies have also found resistance of common bean genotypes to other pests (Silva et al. 2014, Santos et al. 2020b, Shaabani et al. 2021, Zimba et al. 2022). No-choice tests with Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) Middle East Asia Minor 1 described high levels of antibiosis and/or antixenosis in ‘CHIB 06’ (Santos et al. 2020a). Thus, this landrace genotype is an interesting option for smallholders due to its resistance levels to this sucking insect (whiteflies), an emerging insect vector of phytopathogens to beans in field conditions, as well as the resistance to the bruchid-pest of stored beans.

CONCLUSION

Studies on resistance characterization of bean genotypes to A. obtectus are scarce on literature, with a small number of genotypes tested and consequently restricted genetic variability. This background greatly limits breeding programs, highlighting the importance of the present study, as our findings contribute to improving the existing knowledge. Future studies should be carried out to better characterize the resistance types of promising genotypes to A. obtectus, as well as the chemical and morphological factors involved.

ACKNOWLEDGMENTS

We would like to thank professor Edson Luiz Lopes Baldin for all his teachings.

  • How to cite: Cabral, I. R., Baldin, E. L. L., Faria, R. D., Silva, J. P., Santos, T. L. B., Takaku, V. S. O., Santana, A. S., Lima, A. P. S., Canassa, V. F. and Ribeiro, L. P. (2024). Searching for common bean genotypes resistant to Acanthoscelides obtectus, a primary pest species of stored beans. Bragantia, 83, e20230173. https://doi.org/10.1590/1678-4499.20230173
  • FUNDING
    Conselho Nacional de Desenvolvimento Científico e Tecnológico
    Grant No. 310385/2022-9
    Fundação de Amparo à Pesquisa e Inovação de Santa Catarina
    Grant No. 2102/2021
    Fundação de Amparo à Pesquisa do Estado de São Paulo
    Grant No. 2021/05177-2

DATA AVAILABILITY STATEMENT

All dataset were generated and analyzed in the current study.

REFERENCES

  • Acosta-Gallegos, J. A., Quintero, C., Vargas, J., Toro, O., Tohme, J. and Cardona, C. (1998). A new variant of arcelin in wild common bean, Phaseolus vulgaris L., from southern Mexico. Genetic Resources and Crop Evolution, 45, 235-242. https://doi.org/10.1023/A:1008636132108
    » https://doi.org/10.1023/A:1008636132108
  • Adler, C., Athanassiou, C. G., Carvalho, M. O., Emekci, M., Gvozdenac, S., Hamel, D., Riudavets, J., Stejskal, V., Trdan, S. and Trematerra, P. (2022). Changes in the distribution and pest risk of stored product insects in Europe due to global warming: need for pan-European pest monitoring and improved food-safety. Journal of Stored Products Research, 97, 101977. https://doi.org/10.1016/j.jspr.2022.101977
    » https://doi.org/10.1016/j.jspr.2022.101977
  • [Agrofit] Sistemas de Agrotóxicos Fitossanitários (2023). Ministério da Agricultura, Pecuária e Abastecimento. [Accessed on Jan 11 2023]. Available at: https://www.gov.br/agricultura/pt-br
    » https://www.gov.br/agricultura/pt-br
  • Amorim, T. M. L., Macedo, L. L. P., Uchoa, A. F., Oliveira, A. S., Pitanga, J. C. M., Macedo, F. P., Santos, E. A. and Sales, M. P. (2008). Proteolytic digestive enzymes and peritrophic membranes during the development of Plodia interpunctella (Lepidoptera: Piralidae): targets for the action of soybean trypsin inhibitor (SBTI) and chitin-binding vicilin (EvV). Journal of Agricultural and Food Chemistry, 56, 7738-7745. https://doi.org/10.1021/jf801224d
    » https://doi.org/10.1021/jf801224d
  • Athié, I. and Paula, D. C. (2002). Insetos de grãos armazenados aspectos biológicos e identificação. Varela: São Paulo.
  • Avidov, Z., Applebaum, S. W. and Berlinger, M. (1965). Physiological aspects of host specificity in the Bruchidae. II. Ovipositional preference and behaviour of Callosobruchus chinensis (L.). Entomologia Experimentalis et Applicata, 8, 96-106. https://doi.org/10.1111/j.1570-7458.1965.tb00845.x
    » https://doi.org/10.1111/j.1570-7458.1965.tb00845.x
  • Azizoglu, U. (2018). Biochemical properties of Turkish common beans and their resistance against bean weevil Acanthoscelides obtectus (Coleoptera: Bruchidae). Arthropod-Plant Interactions, 12, 283-290. https://doi.org/10.1007/s11829-017-9574-9
    » https://doi.org/10.1007/s11829-017-9574-9
  • Baldin, E. L. L. and Lara, F. M. (2008). Resistance of stored bean varieties to Acanthoscelides obtectus (Coleoptera: Bruchidae). Insect Science, 15, 317-326. https://doi.org/10.1111/j.1744-7917.2008.00216.x
    » https://doi.org/10.1111/j.1744-7917.2008.00216.x
  • Baldin, E. L. L. and Pereira, J. M. (2010). Resistência de genótipos de feijoeiro a Zabrotes subfasciatus (Bohemann, 1833) (Coleoptera: Bruchidae). Ciência & Agrotecnologia, 34, 1507-1513. https://doi.org/10.1590/S1413-70542010000600022
    » https://doi.org/10.1590/S1413-70542010000600022
  • Baldin, E. L. L., Franco, R. S. R. and Souza, D. R. (2007). Resistência de genótipos de feijoeiro Phaseolus vulgaris (L.) a Zabrotes subfasciatus (Boh., 1833) (Coleoptera: Bruchidae). Boletín de Sanidad Vegetal, 33, 369-375.
  • Baldin, E. L. L., Lara, F. M., Camargo, R. S. and Pannuti, L. E. R. (2017). Characterization of resistance to the bean weevil Acanthoscelides obtectus Say, 1831 (Coleoptera: Bruchidae) in common bean genotypes. Arthropod-Plant Interactions, 11, 861-870. https://doi.org/10.1007/s11829-017-9540-6
    » https://doi.org/10.1007/s11829-017-9540-6
  • Baldin, E. L. L., Vendramim, J. D. and Lourenção, A. L. (2019). Resistência de plantas a insetos: fundamentos e aplicações. Piracicaba: FEALQ.
  • Basi, G., Schmid, E. and Maundrell, K. (1993). TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility. Gene, 123, 131-136. https://doi.org/10.1016/0378-1119(93)90552-e
    » https://doi.org/10.1016/0378-1119(93)90552-e
  • Box, G. E. P. and Cox, D. R. (1964). An analysis of transformations. Journal of the Royal Statistical Society, 26, 211-243. https://doi.org/10.1111/j.2517-6161.1964.tb00553.x
    » https://doi.org/10.1111/j.2517-6161.1964.tb00553.x
  • Boyd, D. W., Cohen, A. C. and Alverson, D. R. (2002). Digestive enzymes and stylet morphology of Deraeocoris nebulosus (Hemiptera: Miridae), a predacious plant bug. Annals of the Entomological Society of America, 95, 395-401. https://doi.org/10.1603/0013-8746(2002)095[0395:DEASMO]2.0.CO;2
    » https://doi.org/10.1603/0013-8746(2002)095[0395:DEASMO]2.0.CO;2
  • Cardona, C., Kornegay, J., Posso, C. E., Morales, F. and Ramirez, H. (1990). Comparative value of four arcelin variants in the development of dry bean lines resistant to the Mexican bean weevil. Entomologia Experimentalis et Applicata, 56, 197-206. https://doi.org/10.1111/j.1570-7458.1990.tb01397.x
    » https://doi.org/10.1111/j.1570-7458.1990.tb01397.x
  • Cardona, C., Posso, C. E., Kornegay, J., Valor, J. and Serrano, M. (1989). Antibiosis effects of wild dry bean accessions on the Mexican bean weevil and the bean weevil (Coleoptera: Bruchidae). Journal of Economic Entomology, 82, 310-315. https://doi.org/10.1093/jee/82.1.310
    » https://doi.org/10.1093/jee/82.1.310
  • Carlini, C. R. and Grossi de Sá, M. F. (2002). Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides. Toxicon, 40, 1515-1539. https://doi.org/10.1016/s0041-0101(02)00240-4
    » https://doi.org/10.1016/s0041-0101(02)00240-4
  • Celmeli, T., Sari, H., Canci, H., Sari, D., Adak, A., Eker, T. and Toker, C. (2018). The nutritional content of common bean (Phaseolus vulgaris L.) landraces in comparison to modern varieties. Agronomy, 8, 166. https://doi.org/10.3390/agronomy8090166
    » https://doi.org/10.3390/agronomy8090166
  • Costa, E. N. S., Souza, B. H. S., Bottega, D. B., Oliveira, F. Q., Ribeiro, Z. A. and Boiça Júnior, A. L. (2013). Divergência genética de genótipos de feijoeiro a infestação de Zabrotes subfasciatus (Bohemann) (Coleoptera: Bruchidae). Semina: Ciências Agrárias, 34, 2737-2752. https://doi.org/10.5433/1679-0359.2013V34N6P2737
    » https://doi.org/10.5433/1679-0359.2013V34N6P2737
  • Costa, N. P. and Boiça Júnior, A. L. (2004). Efeito de genótipos de caupi, Vigna unguiculata (L.) Walp., sobre o desenvolvimento de Callosobruchus maculatus (Fabricius) (Coleoptera: Bruchidae). Neotropical Entomology, 33, 77-83. https://doi.org/10.1590/S1519-566X2004000100014
    » https://doi.org/10.1590/S1519-566X2004000100014
  • Ch’ng, L. Z., Barakatun-Nisak, M. Y., Zukiman, W. Z. H. W., Abas, F. and Wahab, N. A. (2019). Nutritional strategies in managing postmeal glucose for type 2 diabetes: A narrative review. Diabetes & Metabolic Syndrome, 13, 2339-2345. https://doi.org/10.1016/j.dsx.2019.05.026
    » https://doi.org/10.1016/j.dsx.2019.05.026
  • Chrispeels, M. J. and Raikhel, N. V. (1991). Lectins, lectins genes and their role in plant defense. Plant Cell, 3, 1-19. https://doi.org/10.1105/tpc.3.1.1
    » https://doi.org/10.1105/tpc.3.1.1
  • Clemente, A., Moreno, F. J., Marín-Manzano, M. D. C., Jiménez, E. and Domoney, C. (2010). The cytotoxic effect of Bowman-Birk isoinhibitors, IBB1 and IBBD2, from soybean (Glycine max) on HT29 human colorectal cancer cells is related to their intrinsic ability to inhibit serine proteases. Molecular Nutrition & Food Research, 54, 396-405. https://doi.org/10.1002/mnfr.200900122
    » https://doi.org/10.1002/mnfr.200900122
  • Dick, K. M. and Credland, P. F. (1984). Egg production and development of three strains of Callosobruchus maculatus (F.) (Coleoptera: Bruchidae). Journal of Stored Products Research, 20, 221-227. https://doi.org/10.1016/0022-474X(84)90007-9
    » https://doi.org/10.1016/0022-474X(84)90007-9
  • Eduardo, W. I., Boiça Júnior, A., Franco, R., Chiorato, A., Perlatti, B. and Forim, M. R. (2016). Antibiosis levels of common bean genotypes toward Zabrotes subfasciatus (Boheman) (Coleoptera: Bruchidae) and its correlation with flavonoids. Journal of Stored Products Research, 67, 63-70. https://doi.org/10.1016/j.jspr.2016.01.006
    » https://doi.org/10.1016/j.jspr.2016.01.006
  • Endshaw, W. and Hiruy, B. (2020). The distribution, frequency of occurrence, and the status of stored faba bean insect pests in relation to food security in Farta District, Northwest Ethiopia. Cogent Food & Agriculture, 6, 1-16. https://doi.org/10.1080/23311932.2020.1832400
    » https://doi.org/10.1080/23311932.2020.1832400
  • Fávero, L. P. and Belfiore, P. P. (2017). Manual de análises de dados: estatística e modelagem multivariada com Excel, SPSS e STATA. Rio de Janeiro: Elsevier.
  • Franco, O. C., Melo, F. R., Silva, M. C. M., and Grossi de Sá, M. F. (1999). Resistência de plantas a insetos: inibidores de enzimas digestivas e a obtenção de plantas resistentes. Biotecnologia, Ciência e Desenvolvimento, 2, 36-40.
  • Franco, O. L., Rigden, D. J., Melo, F. R., Bloch, C., Silva, C. P. and Grossi de Sá, M. F. (2000). Activity of wheat α-amylase inhibitors towards bruchid α-amylases and structural explanation of observed specificities. European Journal of Biochemistry, 267, 2166-2173. https://doi.org/10.1046/j.1432-1327.2000.01199.x
    » https://doi.org/10.1046/j.1432-1327.2000.01199.x
  • Gbaye, O. A. and Holloway, G. J. (2011). Varietal effects of cowpea, Vigna unguiculata, on tolerance to malathion in Callosobruchus maculatus (Coleoptera: Bruchidae). Journal of Stored Products Research, 47, 365-371. https://doi.org/10.1016/j.jspr.2011.06.003
    » https://doi.org/10.1016/j.jspr.2011.06.003
  • Gepts, P. (1999). Development of an integrated genetic linkage map in common bean (Phaseolus vulgaris L.) and its use. In S. Singh (Ed.). Bean breeding for the 21st century (p. 52-92). Dordrecht: Springer.
  • Gonçalves, G. L. P., Ribeiro, L. P., Gimenes, L., Vieira, P. C., Silva, M. F. G. F., Forim, M. R., Fernandes, J.B. and Vendramim, J. D. (2015). Lethal and sublethal toxicities of Annona sylvatica (Magnoliales: Annonaceae) extracts to Zabrotes subfasciatus (Coleoptera: Chrysomelidae: Bruchinae). Florida Entomologist, 98, 921-928. https://doi.org/10.1653/024.098.0317
    » https://doi.org/10.1653/024.098.0317
  • Grossi de Sá, M. F. and Chrispeels, M. J. (1997). Molecular cloning of bruchid (Zabrotes subfasciatus) α-amylase cDNA and interactions of the expressed enzyme with bean amylase inhibitors. Insect Biochemistry and Molecular Biology, 27, 271-281. https://doi.org/10.1016/s0965-1748(96)00093-8
    » https://doi.org/10.1016/s0965-1748(96)00093-8
  • Guedes, N. M. P., Guedes, R. N. C., Silva, L. B. and Cordeiro, E. M. G. (2009). Deltamethrin-induced feeding plasticity in pyrethroid-susceptible and resistant strains of the maize weevil, Sitophilus zeamais Journal of Applied Entomology, 133, 524-532. https://doi.org/10.1111/j.1439-0418.2009.01391.x
    » https://doi.org/10.1111/j.1439-0418.2009.01391.x
  • Guzzo, E. C., Vendramim, J. D., Chiorato, A. F., Lourenção, A. L., Carbonell, S. A. M. and Corrêa, O. M. B. (2015). No correlation of morpho-agronomic traits of Phaseolus vulgaris (Fabaceae) genotypes and resistance to Acanthoscelides obtectus (Say) and Zabrotes subfasciatus (Boheman) (Coleoptera: Chrysomelidae). Neotropical Entomology, 44, 619-625. https://doi.org/10.1007/s13744-015-0315-4
    » https://doi.org/10.1007/s13744-015-0315-4
  • Guzzo, E. C., Vendramim, J. D., Lourenção, A. L., Chiorato, A. F., Carbonell, S. A. M. and Corrêa, O. M. B. (2018). Adult attractiveness and oviposition preference of Zabrotes subfasciatus toward genotypes of common bean Phaseolus vulgaris Phytoparasitica, 46, 645-651. https://doi.org/10.1007/s12600-018-0700-8
    » https://doi.org/10.1007/s12600-018-0700-8
  • Hartweck, L. M., Cardona, C. and Osborn, C. (1997). Bruchid resistance of common bean lines having an altered seed protein composition. Theoretical and Applied Genetics, 95, 1018-1023. https://doi.org/10.1007/s001220050656
    » https://doi.org/10.1007/s001220050656
  • Howe, R., and Currie, J. (1964). Some laboratory observations on the rates of development, mortality and oviposition of several species of Bruchidae breeding in stored pulses. Bulletin of Entomological Research, 55, 437-477. https://doi.org/10.1017/S0007485300049580
    » https://doi.org/10.1017/S0007485300049580
  • Ishimoto, M., and Chrispeels, M. J. (1996). Protective mechanism of the Mexican bean weevil against high levels of α-amylase inhibitor in the common bean. Plant Physiology, 111, 393-401. https://doi.org/10.1104/pp.111.2.393
    » https://doi.org/10.1104/pp.111.2.393
  • Kasahara, K., Hayashi, K., Arakawa, T., Philo, J. S., Wen, J., Hara, S. and Yamaguchi, H. (1996). Complete sequence, subunit structure, and complexes with pancreatic α-amylase of an α-amylase inhibitor from Phaseolus vulgaris white kidney beans. Journal of Biochemistry, 120, 177-183. https://doi.org/10.1093/oxfordjournals.jbchem.a021381
    » https://doi.org/10.1093/oxfordjournals.jbchem.a021381
  • Kljajić, P., Andrić, G. and Golić, M. P. (2023). Evaluation of long-term residual activity of insecticides against Acanthoscelides obtectus (Say) on common bean in laboratory tests. Journal of Stored Products Research, 103, 102156. https://doi.org/10.1016/j.jspr.2023.102156
    » https://doi.org/10.1016/j.jspr.2023.102156
  • Lara, F. M. (1991). Princípios de resistência de plantas a insetos. São Paulo: Ícone.
  • Larson, A. O. and Fisher, C. K. (1938). The bean weevil and the Southern cowpea weevil in California. United States Department of Agriculture, Washington, D.C. Technical Bulletin, 593, 1-70. https://doi.org/10.22004/ag.econ.165798
    » https://doi.org/10.22004/ag.econ.165798
  • Levene, H. (1960). Contributions to Probability and Statistics. Redwood: Stanford University Press.
  • Li, H., Zhou, H., Zhang, J., Fu, X., Ying, Z. and Liu, X. (2021). Proteinaceous α-amylase inhibitors: Purification, detection methods, types and mechanisms. International Journal of Food Properties, 24, 277-290. https://doi.org/10.1080/10942912.2021.1876087
    » https://doi.org/10.1080/10942912.2021.1876087
  • Li, X., Tang, Y., Wang, L., Chang, Y., Wu, J. and Wang, S. (2022). QTL mapping and identification of genes associated with the resistance to Acanthoscelides obtectus in cultivated common bean using a high-density genetic linkage map. BMC Plant Biology, 22, e260. https://doi.org/10.1186/s12870-022-03635-4
    » https://doi.org/10.1186/s12870-022-03635-4
  • Lioi, L. and Bollini, R. (1989). Identification of a new arcelin variant in wild bean seeds. Annual Report of the Bean Improvement Cooperative, 32, 28-29.
  • Lüthi, C., Alvarez-Alfageme, F., Ehlers, J. D., Higgins, T. J. V. and Romeis, J. (2013). Resistance of αAI-1 transgenic chickpea (Cicer arietinum) and cowpea (Vigna unguiculata) dry grains to bruchid beetles (Coleoptera: Chrysomelidae). Bulletin of Entomological Research, 103, 373-381. https://doi.org/10.1017/S0007485312000818
    » https://doi.org/10.1017/S0007485312000818
  • Manly, B. F. J. (2004). Multivariate statistical methods: A Primer. 3. ed. Chapman and Hall/CRC. https://doi.org/10.1201/b16974
    » https://doi.org/10.1201/b16974
  • Mazzonetto, F. and Vendramim, J. D. (2002). Aspectos biológicos de Zabrotes subfasciatus (Boh.) (Coleoptera: Bruchidae) em genótipos de feijoeiro com e sem arcelina. Neotropical Entomology, 31, 435-439. https://doi.org/10.1590/S1519-566X2002000300013
    » https://doi.org/10.1590/S1519-566X2002000300013
  • Mendoza, C. C. and Sánchez, E. (2017). Bioactive compounds from Mexican varieties of the common bean (Phaseolus vulgaris): implications for health. Molecules, 22, 1360. https://doi.org/10.3390/molecules22081360
    » https://doi.org/10.3390/molecules22081360
  • Messina, V. (2014). Nutritional, and health benefits of dried beans. The American Journal of Clinical Nutrition, 100, 437S-442S. https://doi.org/10.3945/ajcn.113.071472
    » https://doi.org/10.3945/ajcn.113.071472
  • Mutungi, C., Chamwilambo, M., Masanja, S., Massam, C., Wayda, P., Tungu, J., Gaspar, A., Bekunda, M. and Abass, A. (2020). Quality and storability of common beans in small-holders farm stores in Northern Tanzania: a multivariate analysis of agro-location, variety, and storage method effects. Journal of Stored Products Research, 89, e101723. https://doi.org/10.1016/j.jspr.2020.101723
    » https://doi.org/10.1016/j.jspr.2020.101723
  • Nadeem, M. A., Yeken, M. Z., Shahid, M. Q., Habyarimana, E., Yılmaz, H., Alsaleh, A., Hatipoğlu, R., Çilesiz, Y., Khawar, K. M., Ludidi, N., Ercişli, S., Aasim, M., Karaköy, T. and Baloch, F. S. (2021). Common bean as a potential crop for future food security: an overview of past, current and future contributions in genomics, transcriptomics, transgenics and proteomics. Biotechnology & Biotechnological Equipment, 35, 759-787. https://doi.org/10.1080/13102818.2021.1920462
    » https://doi.org/10.1080/13102818.2021.1920462
  • Naroz, M. H., Ahmed, S. S., Abdel-Aziz, S. Y. and Abdel-Shafy, S. (2019). First record of Acanthoscelides obtectus (say) (Coleoptera: Chrysomelidae: Bruchinae) in Egypt: development and host preference on five species of legume seeds. The Coleopterists Bulletin, 73, 727-734. https://doi.org/10.1649/0010-065X-73.3.727
    » https://doi.org/10.1649/0010-065X-73.3.727
  • Nassary, E. K., Baijukya, F. and Ndakidemi, P. A. (2020). Intensification of common bean and maize production through rotations to improve food security for smallholder farmers. Journal of Agriculture and Food Research, 2, e100040. https://doi.org/10.1016/j.jafr.2020.100040
    » https://doi.org/10.1016/j.jafr.2020.100040
  • Nazzi, F., Vidoni, F. and Frilli, F. (2008). Semiochemicals affecting the host-related behavior of the dry bean beetle Acanthoscelides obtectus (Say). Journal of Stored Products Research, 44, 108-114. https://doi.org/10.1016/j.jspr.2007.06.004
    » https://doi.org/10.1016/j.jspr.2007.06.004
  • Nchanji, E. B. and Lutomia, C. K. (2021). Regional impact of COVID-19 on the production and food security of common bean smallholder farmers in Sub-Saharan Africa: Implication for SDG’s. Global Food Security, 29, e100524. https://doi.org/10.1016/j.gfs.2021.100524
    » https://doi.org/10.1016/j.gfs.2021.100524
  • Oliás, R., Becerra-Rodríguez, C., Soliz-Rueda, J. R., Moreno, F. J., Delgado-Andrade, C. and Clemente, A. (2019). Glycation affects differently the main soybean Bowman-Birk isoinhibitors, IBB1 and IBBD2, altering their antiproliferative properties against HT29 colon cancer cells. Food & Function, 10, 6193-6202. https://doi.org/10.1039/C9FO01421G
    » https://doi.org/10.1039/C9FO01421G
  • Osborn, T. C., Blake, T., Gepts, P. and Bliss, F. A. (1986). Bean arcelin 2. Genetic variation, inheritance and linkage relationships of a novel seed protein of Phaseolus vulgaris L. Theoretical and Applied Genetics, 71, 847-855. https://doi.org/10.1007/BF00276428
    » https://doi.org/10.1007/BF00276428
  • Paes, N. S., Gerhardt, I. R., Coutinho, M. V., Yokoyama, M., Santana, E., Harris, N., Chrispeels, M. J. and de Sá, M. F. G. (2000). The effect of arcelin-1 on the structure of the midgut of bruchid larvae and immunolocalization of the arcelin protein. Journal of Insect Physiology, 46, 393-402.
  • Parsons, D. and Credland, P. (2003). Determinants of oviposition in Acanthoscelides obtectus: A nonconformist bruchid. Physiological Entomology, 28, 221-231. https://doi.org/10.1046/j.1365-3032.2003.00336.x
    » https://doi.org/10.1046/j.1365-3032.2003.00336.x
  • Paul, U. V., Lossini, J. S., Edwards, P. J. and Hilbeck, A. (2009). Effectiveness of products from four locally grown plants for the management of Acanthoscelides obtectus (Say) and Zabrotes subfasciatus (Boheman) (both Coleoptera: Bruchidae) in stored beans under laboratory and farm conditions in Northern Tanzania. Journal of Stored Products Research, 45, 97-107. https://doi.org/10.1016/j.jspr.2008.09.006
    » https://doi.org/10.1016/j.jspr.2008.09.006
  • Payan, F. (2004). Structural basis for the inhibition of mammalian and insect alpha-amylases by plant protein inhibitors. Bba Proteins and Proteomics, 1696, 171-180. https://doi.org/10.1016/j.bbapap.2003.10.012
    » https://doi.org/10.1016/j.bbapap.2003.10.012
  • Ribeiro, L. P., Vendramim, J. D., Bicalho, K. U., Andrade, M. S., Fernandes, J. B., Moral, R. A. and Demétrio, C. G. B. (2013). Annona mucosa Jacq. (Annonaceae): A promising source of bioactive compounds against Sitophilus zeamais Mots. (Coleoptera: Curculionidae). Journal of Stored Products Research, 55, 6-14. https://doi.org/10.1016/j.jspr.2013.06.001
    » https://doi.org/10.1016/j.jspr.2013.06.001
  • Ribeiro-Costa, C. S., Pereira, P. R. V. and Zukovski, L. (2007). Desenvolvimento de Zabrotes subfasciatus (Boh.) (Coleoptera: Chrysomelidae, Bruchidae) em genótipos de Phaseolus vulgaris L. (Fabaceae) cultivados no Estado do Paraná e contendo arcelina. Neotropical Entomology, 36, 560-564. https://doi.org/10.1590/S1519-566X2007000400014
    » https://doi.org/10.1590/S1519-566X2007000400014
  • Sakthivelkumar, S., Jesse, M. I., Veeramani, V., Ramaraj, P., Kathiravan, K., Arumugama, M. and Janarthanana, S. (2013). Diversity and analysis of sequences encoded by arcelin genes from Indian wild pulses resistant to bruchids. Process Biochemistry, 48, 1697-1705. https://doi.org/10.1016/j.procbio.2013.08.008
    » https://doi.org/10.1016/j.procbio.2013.08.008
  • Santino, S., Valesina, L., Lioi, A., Vitale, A. and Bollini, R. (1991). Bean (Phaseolus vulgaris L.) seed lectins: a novel electrophoresis variant of arcelin. Plant Physiology, 10, 7-11.
  • Santos, T. L. B., Baldin, E. L. L., Ribeiro, L. P., Souza, C. M., Bueno, N. M. and Silva, I. F. (2020a). Silverleaf whitefly-resistant common beans: an investigation of antibiosis and/or antixenosis. Bragantia, 79, 62-73. https://doi.org/10.1590/1678-4499.20190309
    » https://doi.org/10.1590/1678-4499.20190309
  • Santos, T. L. B., Baldin, E. L. L., Ribeiro, L. P., Souza, C. M., Soares, M. C. E., Fanela, T. L. M. and Lourenção, A. L. (2020b). Resistance sources and antixenotic factors in Brazilian bean genotypes against Bemisia tabaci Neotropical Entomology, 50, 129-144. https://doi.org/10.1007/s13744-020-00821-7
    » https://doi.org/10.1007/s13744-020-00821-7
  • Schoonhoven, A. V., Cardona, C. and Valor, J. (1983). Resistance to the bean weevil and the Mexican bean weevil (Coleoptera: Bruchidae) in noncultivated common bean accessions. Journal of Economic Entomology, 76, 1255-1259. https://doi.org/10.1093/jee/76.6.1255
    » https://doi.org/10.1093/jee/76.6.1255
  • Shaabani, J., Hossainzadeh, A., Zeinali, H. and Naghavi, M. R. (2021). A field study on common bean (Phaseolus vulgaris) response to Tetranychus urticae herbivory. Plant Breeding, 140, 464-476. https://doi.org/10.1111/pbr.12914
    » https://doi.org/10.1111/pbr.12914
  • Shapiro, S. S., and Wilk, M. B. (1965). An analysis of variance test for normality (complete samples). Biometrika, 52, 591-611. https://doi.org/10.1093/biomet/52.3-4.591
    » https://doi.org/10.1093/biomet/52.3-4.591
  • Silva, A. G., Boiça Júnior, A. L., Farias, P. R. S., Rodrigues, N. E. L., Souza, B. H. S., Bottega, D. B. and Chiorato, A. F. (2014). Non-preference for oviposition and antibiosis in bean cultivars to Bemisia tabaci biotype B (Hemiptera: Aleyrodidae). Revista Colombiana de Entomologia, 40, 7-14.
  • Smith, C. M. (2005). Plant resistance to arthropods. Dordrecht: Springer Science and Business.
  • Smith, C. M. and Clement, S. L. (2012). Molecular bases of plant resistance to arthropods. Annual Review of Entomology, 57, 309-328. https://doi.org/10.1146/annurev-ento-120710-100642
    » https://doi.org/10.1146/annurev-ento-120710-100642
  • Thakur, D. R. (2012). Taxonomy, distribution, and pest status of indian biotypes of Acanthoscelides obtectus (Coleoptera: Chrysomelidae: Bruchinae): A new record. Pakistan Journal of Zoology, 44, 189-195. https://doi.org/10.13140/RG.2.1.4209.3522
    » https://doi.org/10.13140/RG.2.1.4209.3522
  • Tigist, S. G., Raatz, B., Assefa, A., Melis, R., Sibiya, J., Keneni, G., Mukankusi, C., Fenta, B., Ketema, S. and Tsegaye, D. (2021). Introgression of bruchid (Zabrotes subfasciatus) resistance into small red common bean (Phaseolus vulgaris) background and validation of the BRU_00261 (snpPV0007) resistance marker. Plant Breeding, 140, 1081-1089. https://doi.org/10.1111/pbr.12969
    » https://doi.org/10.1111/pbr.12969
  • Tomé, D. (2013). Digestibility issues of vegetable versus animal proteins: Protein and amino acid requirements: Functional aspects. Food and Nutrition Bulletin, 34, 272-274. https://doi.org/10.1177/156482651303400225
    » https://doi.org/10.1177/156482651303400225
  • Velten, G., Rott, A. S., Cardona, C., and Dorn, S. (2007). The inhibitory effect of the natural seed storage protein arcelin on the development of Acanthoscelides obtectus Journal of Stored Products Research, 43, 550-557. https://doi.org/10.1016/j.jspr.2007.03.005
    » https://doi.org/10.1016/j.jspr.2007.03.005
  • Zaugg, I., Magni, C., Panzeri, D., Gloria, M., Roberto, D., Benrey, B., Bacher, S. and Sparvoli, F. (2012). QUES, a new Phaseolus vulgaris genotype resistant to common bean weevils, contains the Arcelin-8 allele coding for new lectin-related variants. Theoretical and Applied Genetics, 126, 647-661. https://doi.org/10.1007/s00122-012-2008-2
    » https://doi.org/10.1007/s00122-012-2008-2
  • Zimba, K., Sohati, P., Munyinda, K., Kamfwa, K., Roberts, J. and Pope, T. (2022). Evaluation of resistance to black bean aphid (Aphis fabae) in selected varieties and mutant genotypes of common bean (Phaseolus vulgaris). Annals of Applied Biology, 181, 298-308. https://doi.org/10.1111/aab.12776
    » https://doi.org/10.1111/aab.12776
  • Section Editor: Carlos Alberto Scapim https://orcid.org/0000-0002-7047-9606

Publication Dates

  • Publication in this collection
    12 Feb 2024
  • Date of issue
    2024

History

  • Received
    13 Aug 2023
  • Accepted
    16 Nov 2023
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