Legume Research

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Legume Research, volume 45 issue 8 (august 2022) : 933-941

​Advances in Molecular Breeding for Bruchid (Callosobruchus spp.) Resistance in Mungbean [Vigna radiata (L.) Wilczek]: A Review

Prasanta Kumar Majhi1,*, Tanmaya Kumar Bhoi2, Suma C. Mogali3, Aalok Shiv4, Kishore Chandra Sahoo5, Varun Saini6
1Department of Plant Breeding and Genetics, Odisha University of Agriculture and Technology, Regional Research and Technology Transfer Station, Keonjhar-758 002, Odisha, India.
2Division of Forest Protection, ICFRE-Arid Forest Research Institute, Jodhpur-342 005, Rajasthan, India.
3AICRP on MULLaRP, MARS, College of Agriculture, University of Agricultural Sciences, Dharwad-580 005, Karnataka, India.
4Division of Crop Improvement, ICAR-Indian Institute of Sugarcane Research, Lucknow-226 002, Uttar Pradesh, India.
5Department of Agronomy, Odisha University of Agriculture and Technology, Regional Research and Technology Transfer Station, Keonjhar-758 002, Odisha, India.
6Division of Entomology Regional Research, ICAR-Indian Agricultural Research Institute, Pusa, New Delhi-110 012, India.
  • Submitted14-06-2021|

  • Accepted31-08-2021|

  • First Online 11-10-2021|

  • doi 10.18805/LR-4695

Cite article:- Majhi Kumar Prasanta, Bhoi Kumar Tanmaya, Mogali C. Suma, Shiv Aalok, Sahoo Chandra Kishore, Saini Varun (2022). ​Advances in Molecular Breeding for Bruchid (Callosobruchus spp.) Resistance in Mungbean [Vigna radiata (L.) Wilczek]: A Review . Legume Research. 45(8): 933-941. doi: 10.18805/LR-4695.
Mungbean is one of the most important grain legumes with high-quality dietary protein in India as well in many other Asian countries. But the crop is severely affected by bruchids (Callosobruchus spp.) from field to storage condition. These storage pests not only affect the yield but also reduce the market value and quality of the crops. The chemical method of bruchid management is not economical and environmentally unsafe. So, the host-plant resistance to bruchids would be the best alternative and most sustainable way to control the bruchid. A very limited number of wild accessions and cultivated genotypes are available for the transfer of bruchid resistance gene through conventional breeding. Thus, insights into the molecular mechanism of resistance will help to find out the resistance genes/QTLs easily with the support of available genome sequence and that can be introgressed to the cultivated varieties through marker-assisted backcross breeding (MABB) approach. Therefore, in this review, we focused on QTL mapping, identification of novel QTLs, marker assisted-selection, genomics and transcriptomics study by using advanced molecular tools which will be very helpful for genomic-assisted breeding in mungbean for bruchid resistance.
Mungbean [Vigna radiata (L.) Wilczek] is one of the most important legume crops in many Asian countries including India and occupies the third position after chickpea and pigeon pea with respect to area and production. It is a cheap source of dietary protein (24-25%) and carbohydrate (56%) for human consumption (Anonymous, 2016). It plays an important role in sustainable agriculture by increasing the soil fertility through biological N-fixation. The production of mungbean is severely affected by the infestation of pulse beetles (Bruchid; Coleoptera, Bruchidae). Among the bruchids, Callosobruchus maculatus (F.) and Callosobruchus chinensis (L.) cause heavy loss both in the field as well as in the storage (Bharati et al., 2017; Majhi and Mogali, 2020). The initial infestation originates in the field, where the adult beetles lay eggs on green pods and the larva bore through the pod and feed on the developing seed accounting for only 1-2% of damage. When the seeds are stored the insects continue to feed, emerge into adults and cause secondary infestation, which results in the total destruction of seeds within 3-4 months (Bharati et al., 2017; Sanhita et al., 2019).
Several methods are used for bruchid control such as storage under low temperature, solar irradiation of the grains, hermetic storage, use of biocontrol agents, use of botanical extracts and chemical treatment with methyl bromide, carbon disulfide, aluminum phosphide or other substances. Chemical control is effective but increases storage costs, harmful to humans and other animals and hazardous to the environment (Gbaye et al., 2011). Therefore, host-plant resistance to bruchids would be the most sustainable way to control the pest. Bruchid resistance in legumes depends on morphological barriers and secondary metabolites (amino acids, proteins or enzymes) and other toxic compounds interfering with growth, development or reproduction (Edwards and Singh, 2006). Although some sources of resistance have been identified, they are modified at the gene pool level for commercial cultivar release to develop bruchid-resistant mungbean. However, along with the desirable gene, undesired characters may be pronounced in the insect-resistant cultivar (War et al., 2017). To incorporate host-plant resistance in the breeding programs, it needs proper understanding about the lifecycle of bruchid, physical, biochemical and molecular basis of the resistance mechanism. Earlier it was noticed that only hybridization was conducted among the resistant and susceptible lines to transfer the resistant genes. But now due to the advancement of biotechnology, several innovative tools have been developed to study the molecular basis of resistance at the genomics and proteomics level to identify the candidate genes. Studies on bruchid-resistance in relation to the development of molecular markers have gained high thrust by minimizing the dependence on phenotypic data (Chen et al., 2007). The molecular markers for bruchid-resistance have increased the selection efficiency and concurrently reduce the number of selection tests as well as the cost required for screening (Schafleitner et al., 2016). A reliable genome size for achieving the correct coverage and estimating the percentage of repeated sequences of a genome has become an important parameter for planning next-generation sequencing (NGS) experiments (Mao et al., 2016). Therefore, in this review, we are providing insights into the different basis of bruchid resistance in mungbean viz., physical, biochemical and molecular with special attention to the molecular advancement in the direction of breeding programme. Modern plant breeding is dependent on the molecular tools for rapid identification and prediction of genes/ QTLs and introgression of these QTLs. Hence, we focused on i) QTL mapping, ii) identification and annotation of novel genes/QTLs and iii) genomics and transcriptomics study.
Sources of bruchid resistances in mungbean
Among the cultivated Vigna species, only rice bean (Vigna umbellata) is resistant to bruchid. There are only a few bruchid-resistant mungbean varieties available today (Hong et al., 2015) and resistant lines adapted to the tropics are lacking. Recently, several resistant germplasms have been identiûed and used in the breeding programme. Two types of sources that we can get to incorporate the resistance gene into the cultivated species are discussed below:
Wild sources: Resistant but barrier in crossing
The wild accession of mungbean (V. radiata var. sublobata) TC1966 from Madagascar is resistant to many pulse beetles, including C. chinensis, C. maculatus, C. phaseoli and Zabrotes subfasciatus (Tripathy, 2016). A few Australian wild mungbean accessions ACC23 and ACC41 are resistant to C. chinensis, C. maculatus and C. phaseoli (Somta et al., 2007). TC1966 is crossed with V. radiata and the accession of this was introduced into the cultivated gene pool for bruchid resistance (Chen et al., 2013). The resistance factor of TC1966 depends on a single dominant gene (Ishimato et al., 1993; Chen et al., 2013). Sometimes introgression of resistant gene from the crop wild relatives (CWRs) becomes very useful for developing a resistant genotype when the wild accession is cross-compatible to the cultivated ones. Pandiyan et al., (2020) has screened out some introgression lines from RIL population developed from the cross of V. radiata and V. umbellate and also he made intra- and interspecific cross which can be further used for developing bruchid resistant cultivars with improved yield. Even though, few reports are available on the resistance genes, but the practical utility of this information in further breeding is very less. Therefore, proper understanding on the gene at molecular level is most urgent.
Cultivated sources: Available but very less
Bruchid resistance landraces V2709 and V2802 (moderately resistance) subjected to Pure line selection which led to the development of cultivar V2709BG and V2802BG and are highly resistant to both C. chinensis and C. maculatus (Somta et al., 2007). Mungbean accessions (LM 131, V 1123, LM 371 and STY 2633) have been reported to be moderately resistant to bruchid based on the percentage of survival (Somta et al., 2007). It was demonstrated that cultivated mungbean accessions, V2709 and V2802 are highly resistant to C. chinensis and C. maculastus (Somta et al., 2008; Majhi and Mogali, 2020). Majhi and Mogali (2020) conducted an experiment with C. maculatus to screen eight sets of breeding lines of mungbean. They used V-02-802 and V-02-709 as resistant donor for C. maculatus. The result of the cross derivatives of V-02-802 × DGGV-7 and V-02-802 × DGGV-2 were shown resistant responses with a very low susceptibility index of 0.039 and 0.043, respectively as compared to the other breeding lines. The infestation level of C. maculatus is compared among the four genotypes after 45 days of force choice test is given in Fig 1.

Fig 1: Genotypes (a) and (b) are the resistant sources for bruchid species Callosobhuchus maculatus and C. chinensis and commonly used as donor for development of resistant genotype.

Understanding the mechanism of bruchid resistance
Physical basis of bruchid resistance: Determined by shape, size, color and texture of seed and leaf
The first encounter between insect pests and host plants is the antixenosis mechanism of resistance through oviposition. It determines the resistance or susceptibility of the host plants basing on the host genes. Ovipositional probing is necessary for checking host suitability. Any detrimental effect on insect oviposition will have adverse effects on the subsequent generation of pests. Thus the suitability of the host plant determines the nutritional value and the absence of toxic compounds in the host plant will show how good it is for the progeny survival. Many non-preference traits are involved to avoid insect oviposition in both field and storage seeds (Petzold-Maxwell et al., 2011). Mainly biophysical characteristics viz., spines, trichomes, pubescence etc. determine insect oviposition (War et al., 2013). To avoid further infestation by bruchid, the appropriate way to kill the insect eggs are required (Doss et al., 2000). Traits like seed color, texture, hardness, size and chemical constituents mainly contributing to bruchid resistance (Somta et al., 2007; Sarkar and Bhattacharyya, 2015) (Table 1). The oviposition behavior of C. maculatus and C. chinensis are greatly affected by seed texture (Sarikarin et al., 1999). The rough surface of seeds prevents the female bruchid to lay on the seed surface rather than a smooth surface (Watt et al., 1977).

Table 1: Different mechanisms of Bruchid resistance reported in several Mungbean genotypes, mapping populations and accessions.

Biochemical basis of Bruchid resistance: Determined by amino acids, proteins, alkaloids and enzymes
Apart from various morphological characteristics, secondary metabolites are important in defending traits involved in plant defense against insect pests (Wisessing et al., 2008; War et al., 2013). They affect directly on pest biology and show antibiosis mechanism of resistance (War et al., 2012). An array of compounds found in seeds acts either additively or synergistically against insect pests including bruchids. These include vicilins, cysteine rich protein (VrD1 or VrCRP), vignatic acids and para-amino-phenylalanine (Chen et al., 2002; Somta et al., 2007). Mungbean seeds contain lignins, quinines, alkaloids, saponins, non-protein amino acids and polysaccharides and anti-nutritional seed proteins such as lectins, phytohemagglutinins (PHA) and proteinase inhibitors involved in resistance against bruchids. The a-amylase inhibitors interfere with bruchid digestive enzymes and can act as an important biocontrol agent against them (Wisessing et al., 2008) (Table 1). Trypsin inhibitors have been recorded in higher levels in bruchid resistant varieties in mungbean than the susceptible ones (Landerito et al., 1993). Plant lectins are carbohydrate-binding (glyco) proteins that reversibly bind to well-defined simple sugars or complex carbohydrates (Vandenborre et al., 2011). In legumes, lectins are accumulated in seeds and provide a potential defense against bruchids. Canavalin in the seed coat has detrimental effects on the development of bruchids (Oliveira et al., 1999). Two major D-galactose specific lectins (MBL-I and MBL-II) have been characterized by mungbean seeds (Suseelan et al., 1997), but their role in bruchid resistance has not been studied. Lectins from various plants have been reported to alter the growth and development of bruchids (Leite et al., 2005). Lectins such as Canatoxin from Canavalia ensiformis (L.), Zeatoxin from Zea mays seeds, seed lectin from Talisia esculenta Radlk., a galactose-specific lectin from African yam beans, Sphenostylis stenocarpa and a lectin from the marine red alga, Gracilaria ornata Areschoug, has been found highly toxic to C. maculatus (Macedo et al., 2007). They bind to the midgut proteins and reduce the α-amylase activity of C. maculatus larvae (Macedo et al., 2007). Accumulation of cyanogenic glycosides and phytic acid in mungbean seeds during seed maturation plays an important role in defense against bruchids (Lattanzio et al., 2005).
Molecular basis of bruchid resistance: Determined by alleles, genes and QTLs
Various resistance sources of bruchid are reported in wild species in TC1966 and plant breeders utilizing in crop improvement program for the release of resistance variety (Somta et al., 2007). In order to fasten the conventional breeding approach, molecular basis of evidence is necessary against the pest. Source of bruchid resistance in mungbean has been mapped using restriction fragment length polymorphism (RFLP), random amplified polymorphic DNA (RAPD), simple sequence repeat (SSR) and single nucleotide polymorphism (SNP) markers (Chen et al., 2007; Chotechung et al., 2011). TC1966 accession was crossed with susceptible check VC3890 and the F2 population analyzed through restriction fragment length polymorphism. Results revealed that the Br gene has a single locus using linkage group VIII, approximately 3.6 cM from the nearest RFLP marker (Young et al., 1992). Quantitative trait loci (QTL) analysis in TC1966 revealed that one major and two minor QTLs were responsible for bruchid resistance (Chen et al., 2013) (Table 1). A cysteine rich protein VrCPR was identified in TC1966 which shows lethal effect on C. chinensis grub (Chen et al., 2002). The proteomic study suggested that chitinase, beta-1,3-glucanase, peroxidase, provicilin and canavalin precursors play a role in bruchid resistance of mungbean (Khan et al., 2003).
Genomic-assisted resistance breeding
Conventional to molecular breeding: A shift from gene to QTLs
The art of distinguishing desirable traits and incorporating them into future generations is very imperative in Plant breeding. Since the practice of agriculture, farmers have been altering the genetic makeup of the crops unknowingly as they grow. Early farmers selected the best looking plants and seeds and saved them to plant for the next season. Then, once the science of genetics became better understood, plant breeders used what they knew about the genes of a plant to select for specific desirable traits (faster growth, higher yields, pest and disease resistance, larger seeds) to develop improved varieties. Wide hybridization is a reasonable strategy to ameliorate the eroded genetic base of a domesticated crop where the genetic variation is not available within the cultivable germ pool. As we have already discussed that rice bean (V. umbellata) is more resistant to the bruchid hence it can serve as a donor parent for introgressing this bruchid resistance gene in an inter-specific hybridization approach. Mungbean is cross-compatible with rice bean, hence Mathivathana et al., (2019) developed a QTL mapping approach in a RIL population of V. radiata × V. umbellata to unfold the genomic region associated with the bruchid resistance. 108 F3:9-derived lines, developed from the cross of susceptible accession of mungbean VRM (Gg)1 and the resistant rice bean accession TNAU RED, were established as RIL population for this QTL mapping.
Quantitative trait loci (QTL) Mapping: Connecting the genes by molecular markers
QTL mapping includes QTL confirmation, QTL validation and fine (or high resolution) mapping of the genes. Efforts have been made to construct linkage mapping by using RFLP and RAPD markers (Kaga and Ishimoto, 1998) and for studying genetic diversity in mungbean by RAPD along with inter simple sequence repeat profiles (Chattopadhyay et al., 2005). Meng et al., (2015) used QTL mapping and constructed a genetic linkage map. Inclusive composite interval mapping method was used to map the QTL for bruchid resistance (Li et al., 2007). Length of linkage groups and the tightly linked markers can be effectively used in marker-assisted selection, fine mapping and gene cloning. However, further in-depth investigations are needed in this area for developing the stable resistant variety. Kaewwongwal et al., (2017), investigated 77 DNA markers that were located near the Br locus on chromosome 5 of mungbean and screened for polymorphisms between ‘V2709’ and ‘KPS1’ and 19 polymorphic markers were selected to construct a linkage map with a length of 84.12 cM. A single major QTL for C. chinensis (qBrc5.1) and C. maculatus (qBrm5.1) were detected by ICIM (Inclusive composite interval mapping). Results showed that, qBrc5.1 and qBrm5.1 were both located at 34.0 cM, between markers VrID1 and VrSSR017. Results showed that additive and dominant effects of qBrc5.1 were 49.07 and 45.00%, respectively, while those of qBrm5.1 were 48.72 and 44.17%, respectively (Kaewwongwal et al., 2017). Among both QTL alleles, V2709 shows decrease in seed damage caused by bruchids, because both qBrc5.1 and qBrm5.1 were found in the same position and shows similar genetic effects for the resistance.
Kaga and Ishimoto (1998), mapped the ‘Br’ gene by using the RFLP marker in TC1966 and they found that a region of 0.7cM between Bng110 and Bng143. The Br gene is only 0.2 cM away from the Bng143. Chotechung et al., (2011) found that co-segregation of marker DMBSSR158 and Br genes in V2802 as analyzed in expressed sequence tag-simple sequence repeat (EST-SSR) marker. Later, Chotechung et al., (2016) reported a new gene VrPGIP2 showing resistance to bruchid after a complete study of the genomic region of the Br gene that has a fragment of 38 kb segment on chromosome 5, and the VrPGIP2 gene encodes for polygalacturonase-inhibiting protein. Furthermore, some genotypes viz., ‘V2802’, ‘V1128’, ‘V2817’, ‘V2709’ and ‘TC1966’ had the same VrPGIP2 gene activity (Somta et al., 2007). However, further analysis revealed that there is no polymorphism in the EST-SSR marker DMB-SSR158, which is located on the VrPGIP2 sequence, in genotype ‘V2709’ and bruchid-susceptible mungbean ‘Kamphaeng Saen 1’ (Chotechung et al., 2011).  This information suggested that the gene or allele for bruchid resistance in ‘V2709’ is different from that of ‘V2802’.
Development of markers accompanying with bruchid resistance genes
Traditionally available markers were not proved quantifiable information for resistance, so more information is needed on Br gene linked reliable markers for the breeding of bruchid-resistant mungbean varieties. Br gene usually associated with molecular markers associated with mapping the resistance genes that help to identify the factors underlying resistance against bruchids. Studies shown that gene-based or regulatory sequence-based markers could be efficient for this breeding program. Locus-linked RFLP and RAPD markers were also found more reliable for the selection. Resistance factors may occur because of changes in biochemical activity in susceptible and resistant lines, due to sequence variation or from expression differences of resistance genes. Polymorphic differences in resistant genes would provide reliable markers for resistance (Mao-Sen et al., 2016). The whole-genome sequence of a bruchid susceptible mungbean (V. radiata var. radiata VC1973A) was investigated in RILs population and annotates 14,500 genes (Kang et al., 2014). They also identified differentially expressed genes (DEGs) and nucleotide variations (NVs) in the promotor regions of DEGs and in the exons of sequence-changed protein genes (SCPs). The putative effects of DEGs and SCPs on bruchid resistance of mungbean were discussed and studies confirm that molecular markers derived from NVs could be used further for the selection of resistant lines (Kang et al., 2014). Mao-Sen et al., (2016) had identified linked markers (g779p, g34480p and g34458p) for resistant reaction from a RIL population between resistant and susceptible lines. Studies revealed that newly developed markers like g779p and g34480p exhibited 93.4% accuracy, which is far better than g34458p. Further studies confirmed with two bruchid-resistance-associated markers, the CAP marker OPW02a4 and SSR marker DMB-SSR158 (Chen et al., 2007; Chen et al., 2013) in 61 RILs revealed that, marker DMB-SSR158 shows the highest accuracy of 98.3% in bruchid resistance mungbean.
Genome-transcriptome analysis: Searching novel alleles and gene annotation
The genome-transcriptome comparison study was carried out by Mao-Sen and co-workers (2016) for bruchid-resistance-associated genes by comparing the seed transcriptome of bruchid resistant (R) and susceptible (S) mungbean lines of two parental populations of NM92 (S) and TC1966 (R) and derived RILs. Two methods to RNA-seq were used for identifying DEGs. In the first approach, the number of transcripts per million (TPM) was calculated, results revealed that 22 up- and 6 downregulated genes were found in seeds of bruchid-resistant mungbean. Three upregulated genes namely g4706, g34480 and g42613 were detected in R-mungbean and two downregulated genes viz., g40048 and g41876 were detected in S-mungbean. In the second approach, DESeq analysis and total nine transcriptomes have identified 81 transcripts of 80 DEGs. Results show that a total of 31 were up- and 49 downregulated in bruchid-resistant mungbean. Furthermore, downregulated gene g16371 was present in two splice forms, g16371.t1 and g16371.t2 (Chen et al., 2002). Further studies confirmed that 10 genes (g24427, g34321, g4706, g34480, g28730, g17228, g9844, g39181, g39425, g42613) were expressed only in bruchid resistant lines and three (g40048, g35775, g2158) were found in bruchid-susceptible lines (Mao-Sen et al., 2016).
Studies conducted by Chotechung et al., (2016) shown that, VrPGIP2 is an intronless gene. It has 1,011 nucleotides and it translates into a 336-amino acid protein, which is similar to gene LOC106760237 annotated by NCBI. Sequence alignment of VrPGIP2 genes from ‘V2802’ and KPS1 shows that seven SNPs (at nucleotide positions 573, 958, 969, 972, 995, 1,003 and 1,008) present between the two mungbean accessions (Kaewwongwal et al., 2017). VrPGIP1gene was annotated by Kang et al., (2014) and it had three exons with an open reading frame of 1,302 nucleotides that encodes a 433-amino acid protein (Chotechung et al., 2016). However, the current mungbean genome annotation by NCBI showed that VrPGIP1 (LOC106760236) is intronless, has 1,011 nucleotides and encodes a 336-amino acid protein, which is the same as VrPGIP2. Finally two new alleles named VrPGIP1-1 and VrPGIP2-2 were identified by sequencing VrPGIP1 and VrPGIP2 genes respectively from mungbean accession ‘V2709’ (Kang et al., 2014; Kaewwongwal et al., 2017). Again a recent finding by Kaewwongwal et al., (2020) revealed a second allele for VrPGIP1 from ACC41, the resistant wild accession of mungbean (V. radiata var. sublobata).
Phenotypic selection needs special environmental conditions, if the environment is not suitable then there may be a chance that the susceptibility may not come for screening and selection, so the breeder may lose a season for it. Phenotypic based selection is also time-consuming, tedious, laborious and may be expensive. As the phenotypic data is environmentally sensitive, so it is necessary to use the molecular markers along with continuous backcrossing to increase the efficiency of selection and to reduce the number of selection tests as well as the cost required for screening. But, the selection through molecular markers shows more reliability in selection as it is not affected by the environment. Marker-assisted selection is genome-specific in nature, shows clear distinct allelic features, no detrimental effects on phenotypes and; easy assay and automation. A comparison between conventional and genomic-assisted plant breeding approach for the development of mungbean genotypes resistant to bruchid is given in Fig 2. The development of successful bruchid resistance genotype in mungbean has attracted the attention of Plant Breeders, Entomologists and Biotechnologists due to its severe loss during storage. It is necessary to understand the developmental biology of bruchid before trying to access the resistance in the host genotype. The identified Br locus related molecular markers should validate properly to use in further breeding programme. Regulatory sequence-based or gene-based molecular markers would be the best for selecting bruchid resistant lines. Even though some resistant genotypes are identified for cultivation but still more research is necessary to give a sufficient number of resistant varieties to the farming society. Although some sources of resistance to bruchids are identified and used for crossing with high yielding varieties the difficulty is the transfer of undesirable characters with the resistance gene. Studies on bruchid resistance in relation to the development of molecular markers have gained high momentum. Further, bruchid resistance from black gram can be transferred into mungbean eficiently using interspecific or intraspeciûc crosses supported by bruchid resistance gene markers. RFLP and SSR markers have been widely used for mapping the bruchid-resistant gene in mungbean, owing to its complicated protocol to identify the resistance genes governing the trait. Due to the evolutionary force, bruchids may acclimatize to the newly formed resistant lines with single-gene resistance; thus, there is a prerequisite to identify and combine multiple resistant genes into the same cultivar through gene pyramiding strategies.

Fig 2: An illustration between (a) conventional plant breeding and (b) genomic-assisted plant breeding approach for the development of mungbean genotypes resistant to bruchid.

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