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Breeding for Resistance to the African Sweetpotato Weevils, Cylas puncticollis and Cylas brunneus in Uganda: A Review of the Current Progress

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01 September 2023

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05 September 2023

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Abstract
In sub-Saharan Africa, sweetpotato weevils are the most devastating pests of cultivated sweetpotato, causing estimated losses of between 60% and 100%, primarily during dry spells. The predominantly cryptic feeding behavior of the Cylas spp within the roots makes their control difficult, thus host plant resistance is one of the most promising lines of protection against these pests. However, progress in breeding for weevil-resistant cultivars has been slow in part due to the complex hexaploid genome of sweetpotato, which complicates conventional breeding in addition to the scarcity of varieties with significant levels of resistance for use as sources of resistance. Pollen sterility, cross incompatibility and poor seed set and germination in sweetpotato are also common challenges to improving weevil resistance. Accurate phenotyping of sweetpotato weevil resistance to enhance efficiency of selection has been equally difficult. Genomics-assisted breeding though in its infancy stages in sweetpotato has the potential application in overcoming some of these barriers. However, it will require the development of more genomic infrastructure; particularly single nucleotide polymorphism markers (SNPs), robust next generation sequencing plat-forms together with relevant statistical procedures for analyses. With the recent advances in genomics, we anticipate that genomic breeding for sweetpotato weevil resistance will be expedited in the coming years. This review sheds light on Uganda's efforts to date to breed against the Cylas puncticollis (Boheman) and Cylas brunneus (Fabricius) species of African sweetpotato weevil.
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Subject: Biology and Life Sciences  -   Insect Science

1. Introduction

Sweetpotato (Ipomoea batatas (L.) Lam.) (2n = 6x = 90) is the third most important root crop in the world after potato and cassava, with an estimated total global production of 88.7 million metric tons [1]. It is one of the major staple foods in sub-Saharan Africa (SSA), where it ranks as the second most important root crop after cassava. Africa is currently the 2nd largest sweetpotato producing continent, after Asia, with an estimated annual production of 28.6 million metric tons accounting for 32% of the total worldwide production [1]. This clonally propagated crop is part of the Convolvulaceae family and is the only economically important species of the Ipomoea genus [2].
Sweetpotato is predominantly cultivated by small holder farmers through subsistence farming in Uganda. Its importance in the region is mainly attributed to its contribution to food security and income generation for marginalized farmers [3]. Sweetpotato is known to possess a wide range of nutrients including carbohydrates (21%), fibre (3.3%), minerals (potassium, copper and manganese) and vitamins such as vitamin A, B6 and C [4]. The orange-fleshed genotypes are particularly known to be an important source of β-carotene, a precursor for vitamin A and are making a significant contribution towards alleviating vitamin A deficiency in SSA particularly among children and pregnant women [5,6]. Many farmers in Uganda and the region like it as a crop because of its ability to generate high yields in relatively poor soils with minimum inputs and its resistance to a variety of biotic and abiotic stresses [5,7].
Sweetpotato weevils (SPWs) Cylas spp., are the most destructive pests of sweetpotatoes in Uganda and the SSA region, causing estimated yield losses of between 60% and 100% [8,9,10], mainly during dry spells and under heavy infestations. Cylas puncticollis (Boheman) and Cylas brunneus (Fabricius) are the predominant species occurring in Africa [8,11]. They attack the leaves, stems, and storage roots of sweetpotatoes, resulting in poor quality roots with an unacceptable smell and bitter taste due to secretion of defense sesquiterpenes by the infested plants, that makes the roots unfit for human and livestock consumption [12,13].
The concealed feeding behavior of weevils within storage roots makes them quite challenging to control by methods such as chemical control. Host plant resistance, therefore, presents a more suitable alternative for the integrated pest management (IPM) of this pest. Sweetpotato breeding, however, remains a difficult task due to the large and complex nature of its genome, with additional limitations such as self and cross incompatibility, limited flowering ability and seed setting [14], which further complicate conventional breeding.
The development of SPW resistant varieties has been unsuccessful to date, owing to a lack of high heritable resistance in the sweetpotato germplasm evaluated in the past [3,15]. However, some landraces with moderate resistance have previously been identified and researchers are currently using these as parental materials in an effort to develop resistant varieties [16,17]. Genomic selection and marker assisted selection stand out as promising options for developing SPW resistant varieties in Uganda [17]. This review gives an insight into the progress that has so far been made in breeding for resistance to the African sweetpotato weevils, Cylas puncticollis (Boheman) and Cylas brunneus (Fabricius) in Uganda. It also highlights aspects relating to the management and control of the two Cylas species.

2. Taxonomy and Geographical Distribution of Cylas species

Sweetpotato weevils (Cylas spp.) belong to the Order Coleoptera, Brentidae family and Cyladinae subfamily [18]. They are divided into three groups; C. brunneus, C. puncticollis and C. formicarius, which vary in physical characteristics such as body shape, length of the hind femora, head structure, and genitalia features [8]. Cylas formicarius is typically an Asian species but occurs throughout the tropical and sub-tropical regions of the world including Asia, Europe, North America and Africa [19]. Cylas puncticollis and Cylas brunneus however, are restricted to Africa [8,20]. They are the most prevalent and commonly reported SPW species on the continent [16,21,22,23]. Cylas puncticollis in particular, is the most abundant in tropical Africa, reported in 24 African countries, including Uganda, Rwanda, Ghana, Nigeria, DR Congo, Kenya, Malawi, Cameroon and Ethiopia [13,24].

3. Description and Life cycle of Cylas species

Adult females of Cylas species usually lay their oval, yellowish eggs singly in a cavity excavated either in sweetpotato roots or stems, which they subsequently seal with faecal plug [25]. Roots are the most preferred oviposition sites and most eggs tend to be deposited near the crown of the root. Duration of the egg stage varies from 5 to 12 days, with eggs of C. puncticollis developing faster than those of C. brunneus [26]. The larvae of Cylas spp. are usually curved in shape and white in color, feeding and developing within the stems and roots of sweetpotato. Pupae are glabrous in shape, with those of C. puncticollis being relatively larger than C. brunneus [25] (Figure 1). Male and female adults of both species can be differentiated by the shape of the distal antennal segment, which is filiform in males and club like in females [18]. The two species Cylas spp. differ in morphology, coloration and general development (Table 1).

4. Host Range and Dispersal of Cylas species

Sweetpotato is the preferred host plant for C. puncticollis and C. brunneus. In Uganda, the demand for additional hosts for weevil survival may not be as great because most cropping systems allow for year-round sweetpotato production. On the other hand, other Ipomoea species do not produce swollen roots, which provide oviposition sites; hence, population build up may be very low. Sweetpotato weevils usually get dispersed by flying and crawling, with males being more agile and flying more than females [12,25]. Long-distance dispersal however, is mostly through the movement of infested sweetpotato storage roots and vines [13].

5. Damage Caused by Cylas species

Cylas spp damage the leaves, stems and storage roots of sweetpotato. Adults injure the vines and leaves by feeding on the epidermis, scraping and creating oval patches, which may lead to a significant reduction in plant vigor and poor establishment in case of early infestation [8]. Larvae usually damage the stem by feeding at the base, thereby affecting the vascular system, causing the vines to swell and eventually wilt or die [13]. However, the most significant damage is inflicted when weevils attack the underground storage roots. Adults feed on the external root surfaces causing feeding punctures, which can be distinguished from oviposition sites by their greater depth and the absence of faecal plug [27]. Larval feeding and tunneling creates irregular galleries in the inner part of the root or stem, further damaging the plant (Figure 2). In response to this, the roots produce sesquiterpenes in self-defense, which give the root an unacceptable odour and bitter taste, rendering them unsuitable for consumption either as food or animal feed [13,15]. The damage caused by Cylas spp therefore affects the quantity, quality and value of sweetpotato storage roots produced. Losses of commercial storage root yield as high as 60–100% have been reported under heavy infestations in SSA [8,28].

6. Management and Control Strategies

A number of agricultural practices have been suggested for the management and control of SPWs (Table 2). Because none of them is completely effective in the control of this elusive pest, an integrated pest management (IPM) approach is usually recommended. Control is made difficult because all immature developmental stages of Cylas spp. occur deep inside the storage roots and stems of the plant [13].

7. Mechanisms of resistance of sweetpotato to Cylas spp.

Different resistance mechanisms found existing in sweetpotato germplasm against the SPW have previously been reported including antibiosis, antixenosis, and escape [44]. Other studies demonstrated that SPW resistance is more than simply an escape mechanism through field phenology such as deep rooting plants, but rather an active mechanism that is quantifiable and potentially manageable for breeding purposes [3,15,23]. Hydroxycinnamic acid (HCA) esters in the root latex and root surface (epidermal and peridermal tissues) of sweetpotatoes were shown to deter the development of SPW larvae, reducing feeding damage and oviposition. The HCAs were identified as heptadecylcaffeic acid, hexadecylcaffeic acid, octadecylcaffeic, hexadecylcoumaric acid, octadecylcoumaric acid and 5-0-caffeoylquinic acids from Ugandan sweetpotato varieties “New Kawogo” and “Tanzania” [15,16,17]. These acids are a major group of phenolic compounds with bioactive properties that are produced by plants for protection against biotic and abiotic stress [45].

8. Progress in breeding for resistance to Cylas spp.

Progress in breeding for sweetpotato weevil resistance has been rather slow due to factors such as the complex nature of the sweetpotato genome and the limited sources of genetic resistance to Cylas spp [3,15]. Genetic studies in sweetpotato are limited by high levels of self and cross-incompatibility, limited flowering ability, high ploidy levels and poor seed germination as also observed in Taiwan [46]. Each successful cross usually leads to the production of less than three botanical seeds [47]. This makes conventional breeding that relies only on hybridization to create genetic variability, a challenge.
Nevertheless, the breeding program at the National Crops Resources Research Institute (NaCRRI) in Uganda, has in the past and to-date, used conventional breeding and population improvement through recurrent mass selection for variety development in Uganda [48,49]. The phenotyping of SPW resistance was based on severity and incidence estimations. Sweetpotato severity was routinely assessed using standard protocols and a scale of 1-9 was employed where 1 = no weevil damage symptoms, 2 = unclear weevil damage symptoms, 3 = clear weevil damage symptoms < 5% of roots per plot, 4 = clear weevil damage symptoms at 6 to 15% of roots per plot, 5 = clear weevil damage symptoms at 16 to 33% of roots per plot, 6 = clear weevil damage symptoms in 34 to 66% of roots per plot (more than 1/3, less than 2/3), 7 = clear weevil damage symptoms in 67 to 99 % of roots per plot (2/3 to almost all), 8 = clear weevil symptoms in all roots per plot, 9 = severe weevil damage symptoms in all roots per plot (rotting) [96]. Incidence of sweetpotato weevil damage was measured as a percentage of number of storage roots showing weevil damage symptoms to the total number of roots in a plot.
In the past, sweetpotato morphological traits such as vine vigor, ground cover, foliage weight, storage root stalk (neck length), storage root cortex thickness, storage root size, storage root shape, storage root formation (arrangement), root latex production, and dry matter content were reported to play an important role in conferring field resistance to SPW [41]. But through correlation and path coefficient analysis, neck length was identified as the key morphological SPW resistance predictor [50]. This trait will be useful in selecting for SPW resistance among breeding clones during early stages of breeding. This could be done at a single site before advancing clones for multi-location evaluation and analysis of biochemical hydroxycinnamic acids, thereby minimizing research costs.
To date, the National Crops Resources Research Institute of the National Agricultural Research Organization (NARO) has released 29 sweetpotato varieties of varying levels weevil resistance in Uganda [97-102]. All the 29 sweetpotato varieties that have been released in Uganda so far are either moderately resistant or susceptible to sweetpotato weevils (Table 3). Varieties like “New Kawogo”, which express moderate resistance to Cylas spp. are currently deployed as parental material in SPW breeding and related studies in Uganda [15].

9. The genetic and biochemical basis for sweetpotato weevil resistance

The development of sweetpotato varieties with resistance to SPWs requires an understanding of the underlying biochemical and genetic mechanisms of resistance to this pest. Our understanding of the genetic and biochemical basis of resistance to SPWs has been improved in the past decade through a number of studies. Previous research conducted to determine the basis of weevil resistance in the Ugandan landrace, “New Kawogo”, to the African SPW C. puncticollis revealed that resistance in this variety was not only active, but also quantifiable and manageable for breeding [15]. In another study, 134 sweetpotato cultivars and landraces were evaluated for weevil resistance. Some sweetpotato cultivars, including “New Kawogo”, expressed resistance to Cylas spp. while others such as “Tanzania” and “NASPOT1” turned out to be susceptible [23].
In order to identify the biochemical basis of resistance to SPWs, the performance of seven resistant varieties of sweetpotato were compared with three susceptible varieties in field trials and laboratory bioassays [16]. Using liquid chromatography-mass spectrometry (LC-MS) of root surface and epidermal extracts, significant variation in the concentration of hexadecyl, heptadecyl, octadecyl, and quinic acid esters of caffeic and coumaric acid were exhibited, with higher concentrations of these compounds correlated with SPW resistance. “New Kawogo” recorded the highest concentration of these compounds. It was therefore concluded that the selection of sweetpotato varieties with higher levels of HCAs, particularly in the storage root surface, would probably contribute to the development of resistance to SPWs. However, this would necessitate the screening of hundreds of breeding lines using freeze-dried samples of roots and analysis by LC-MS in order to achieve long-term population improvement. Developing such a chemotyping platform, though desirable, would be quite costly [17].
In a further effort to understand the segregation of HCA esters that confer resistance to SPWs, Anyanga, et al [3] quantified these chemicals among 287 progenies of a segregating bi-parental population of the “New Kawogo” x “Beauregard” (NKB) cross. Beauregard is a USA-released cultivar, highly susceptible to SPWs. Results revealed that HCA esters conferred resistance to SPWs and segregate in the F1, suggesting that they are controlled quantitatively, and thus, might be useful as markers for resistance in sweetpotato breeding programs. The progeny that displayed more resistance to SPWs than “New Kawogo”, together with those that had higher concentrations of HCA esters, were selected as new candidates and are currently being utilized as parental genotypes in sweetpotato breeding.
Knowledge on the inheritance and heritability of resistance to the African SPWs is also apparently still limited. Some studies have been done in the past to establish the heritability of SPW resistance in which resistance to Cylas spp. was measured on the basis weevil severity of field storage roots and total HCA ester concentrations [17]. A moderately high broad sense heritability was estimated (H2=0.49). Another study revealed similar results (with H2=0.49%) and further showed that additive effects contributed the most to SPW resistance and HCA concentration [51]. More recently, a narrow sense heritability (h2=0.30) was reported for SPW resistance based on a relatively high population [52]. We hope that the adoption of modern experimental designs such as the row-column designs, which use more replications for field phenotyping, will enable estimation of higher heritability values for SPW resistance for future genomic analyses.

10. Marker assisted selection and Genomic selection for SPW resistance

The limited number of genomic resources has been a major bottleneck in breeding for SPW resistance. Over the years, sweetpotato genomic improvement has generally lagged behind other important crops such as maize [53], rice [54] and wheat [54]. This has been attributed to the scarcity of molecular markers to facilitate genetic analyses [55], lack of appropriate specific statistical procedures due to its polyploid nature, and limited user-friendly computer software to implement the statistical procedures for genetic analyses of important traits [56]. Sweetpotato was termed as an “orphan crop” with limited private investment in the development of its genomics infrastructure [56]. Nevertheless, to maximize the success rate in developing sweetpotato varieties, genomic tools are critical [57], particularly since most traits in sweetpotato are quantitatively inherited [55,58].
Molecular markers have hardly been used in sweetpotato genetic research compared to other staple crops yet they are critical in the genetic analysis of complex traits [55,59] and increase the efficiency of selection for low heritability traits through marker assisted selection (MAS) [55,59].
Sweetpotato weevil resistance, like most sweetpotato traits of agronomic and economic importance is quantitative in nature; controlled by many genes and with high environmental plasticity [46,51]. This has resulted in slow breeding progress through the use of conventional breeding approaches. Associating such a complex trait to genomic regions can be done through Quantitative Trait Loci (QTL) analysis [59]. However, there is currently a low number of published SSR and SNP markers for sweetpotato [17,51,60,61]. In the past, most molecular genetic studies in sweetpotato were based on dominant markers such as random amplified Polymorphic DNA (RAPDs) and amplified fragment length polymorphisms markers (AFLPs) that are relatively easy to score [62,63,64]. However, these QTLs have limited utility and cannot be used for sweetpotato improvement by MAS and genomic selection (GS). Simple sequence repeats (SSR) and single nucleotide polymorphism markers (SNPs), which are amenable to automation, are more suitable for sweetpotato breeding through MAS [17,65].
Some initial progress has been made in identifying SSR and SNP markers for use in breeding for SPW resistance. Yada et al [66] conducted a study in which he examined the genetic diversity in the NKB population using SSR markers. Sweetpotato SSR markers (405) were screened for polymorphism on the parents and progeny of the biparental cross. A total of 133 SSRs were identified as informative and recommended for use in further sweetpotato diversity and linkage analysis. The same population was later genotyped with these SSR markers to identify SPW resistance loci [17]. Five SSR markers were observed to be associated with field SPW severity whereas seven were linked to HCA ester concentration. Three markers showed significant association, suggesting their high potential for use in the development of SPW resistant cultivars [17]. This was the first report of co-dominantly inherited SSR markers being utilized to identify SPW resistance loci in sweetpotato in Uganda. Next-generation sequencing (NGS) technology and a genotyping by sequencing approach was later used to develop SNP markers and high-density genetic linkage maps using the NKB population [51]. This led to the identification of 4 QTL, explaining a total of 37.7% of the variation for SPW resistance and 15.9% of the variation for storage-root HCA ester concentration in the mapping population. This was the first report of a QTL mapping study for resistance to SPWs and HCA ester concentration [51].
Genomic selection stands out as a novel approach to accelerate genetic gains in sweetpotato [67]. In their pioneering work to explore the potential of genomic selection on sweetpotato, the predictive ability based on several factors was done for simple traits and yield traits for a single population. Though the predictive ability was low for complex traits, the use of multi trait models offered confidence for better prediction of such traits [67]. In addition, studies in other polyploids like octaploid strawberry, have reported high accuracy for lower heritability traits [68,69]. Despite the reports of lower heritability for insect pest resistance across crop species, the application of genomic prediction in maize showed moderate to high predictive ability for fall army worm and maize weevil [70]. Therefore, the application of genomic selection for weevil resistance is feasible and can be achieved after optimizing the size, composition, structure and phenotyping of training population and assembling sufficient diversity in the population.

11. Genomic resources for sweetpotato improvement

Through global collaborative research, high quality sequencing of the genomes of two diploid close relatives of sweetpotato, I. trifida and I. triloba, was successfully accomplished [71] and a genome sequence-based marker platform for sweetpotato improvement was developed. Ipomoea trifida is the closest wild species to sweetpotato, as evidenced by a number of cytology and molecular studies [72,73,74,75]. Though it’s the preferred reference for I. batatas, the I. triloba genome can also be used as a complementary reference sequence in sweetpotato breeding [71]. Although another sweetpotato reference genome was released by Yang et al [76] and later on improved, efforts are still underway to develop a high quality whole genome sequence for hexaploid sweetpotato [77,78]. Once completed, this will facilitate genomic selection and enable more efficient introgression of important traits such as SPW resistance, ultimately leading to the development of sweetpotato varieties with desirable attributes.
The advances in DNA sequencing methods through next-generation sequencing (NGS) technology and bioinformatics resources over the past decade have enabled large numbers of SNP markers to be developed and utilized [77,78]. Genome wide association studies (GWAS), which investigate the association between genotypes and phenotypes using the entire genome, have also been facilitated by the development of NGS techniques. Through GWAS, existing phenotypic and/or genotypic data can be utilized from larger population sizes to produce higher statistical power in analysis provided that a sufficient marker density is available [77].

12. Genetic transformation for weevil resistance

Research has been done in SSA to develop varieties that are resistant to SPWs through genetic transformation and crossing landraces with transgenic cultivars. Transformation for weevil resistance was among the first that were attempted in sweetpotato [57]. Sweetpotato cultivar ‘KB1’ was transformed with a delta endotoxin gene cry8Db, acquired from Bacillus thuringiensis via Agrobacterium mediated transformation. This gene codes for an insecticidal protein that is lethal to many insect larvae. The 21 transgenic lines that were regenerated from the transformed calli displayed lower SPW infestation compared to the untransformed lines [78]. Agrobacterium mediated transformation was similarly used to transform ‘Kyebandula’, a Ugandan sweetpotato landrace, by introducing two bacterial endotoxin genes cry7A1 and cry3Ca. The process was reportedly successful as evidenced by positive PCR results. However, transformed calli were unable to regenerate into whole plants [79].
Ekobu et al [80] conducted an experiment in which they evaluated the toxicity of Cry proteins to C. puncticollis and C. brunneus. The three most active Bt Cry proteins, with potential to confer resistance against C. puncticollis and C. brunneus, were Cry7Aa1, cryET33-34 and Cry3Ca1 with an LC50 value (mg/ml diet) against the first instar C. puncticollis and second instar C. brunneus below 1 ppm. However, they did not show efficacy against the weevil, a result partly ascribed to the low level of Cry protein expression in the root tissue. In another study, the feasibility of crossing transgenic and non-transgenic sweetpotato to obtain transgenic progeny was explored [7]. However, there were no significant differences in Cry protein expression among hybrid sweetpotato derived from the transgenic event crossed to different conventional sweetpotato varieties. Transgenic sweetpotato expressing Cry proteins did not perform with the desired levels of resistance to C. puncticollis. The study recommended evaluation of more transgenic events carrying Cry proteins to increase the possibility of finding those with higher Cry protein accumulation.
Recently, Anyanga et al [81] studied the effect of combining the anti-feedant effects of HCA esters with expression of Bt proteins in transformed plants. The study observed that although resistance was naturally conferred by HCA acids, and deterred oviposition by adults, these compounds were restricted to the roots and did not protect against the larvae, which feed in the cortex, causing the greatest damage. The authors evaluated the bioactivity of Cry7Aa1 protein and HCA esters both individually and in combination for causing mortality against SPW larvae. Larval mortality proved to be higher when a combination of HCA esters and Bt protein was used under laboratory bioassay conditions. Further research was recommended to establish the effect of the combination under field conditions.

13. Future Prospects

Further research on genetic transformation and genome editing: The evaluation of more transgenic events carrying cry genes would increase the likelihood of successfully identifying those with higher cry protein expression, which could potentially provide effective weevil control. Mitigating any existing bottlenecks in genetic transformation could provide a major breakthrough in genetic improvement of sweetpotato. The use of RNAi technology that has been tested on the African sweetpotato weevil species [82,83]offers a future potential for managing this pest in Uganda. Nevertheless, it is time to apply modern approaches such as gene editing in sweetpotato for sweetpotato weevil management.
Improved phenotypic strategies and analytics: As sequencing and genotyping costs continue to drop, phenotyping has been highlighted as one of the most expensive and major limitations to the accurate mapping of traits in plant breeding [84]. Novel next generation phenotyping platforms that facilitate accurate, low cost and timely acquisition of phenotypic data [85] will need to be developed and utilized for enhancing the quality of phenotypic data collected in Uganda and the region. High-throughput, near-infrared reflectance spectroscopy (NIRS) analysis of root chemistry composition, which has been implemented in many breeding programs [84], will need to be adopted and scaled out in the SSA region. Many imaging platforms and computer software have been developed for automated screening of attributes such as root and leaf architecture [86,87,88]. However, most of these modern phenotyping platforms have not been implemented in sweetpotato research in Uganda, where SPW severity is currently measured by visual assessment of damage symptoms on roots [89]. Additionally, the application of modern analytics is vital to maximizing phenotypic data outputs. For instance, the use of modern experimental designs such as the row column designs, which cater for more replications for field phenotyping, and analysis of data using mixed models would enhance heritability values for the genomic analyses.
Advances in plant bio-chemistry: Advances will need to be made in the use of plant biochemistry for revealing the basis of pest resistance in sweetpotato. Although plant biochemistry is now being used for screening for SPW resistance in Uganda breeding program, low-cost analysis throughput platforms such as near-infrared spectroscopy (NIRS) are needed since chemical profiling of resistance by wet chemistry platforms such as liquid-chromatography mass spectrometry (LC-MS) are still expensive for the breeders who screen large numbers of clones at the various breeding stage gates. The calibration of NIRS for analysis of total HCA ester concentrations in root samples would enhance throughput screening of breeding materials for population improvement [17]. This could be plausible considering that a similar method, fourier-infrared spectroscopy, has previously successfully been used for quantification of total HCA esters in forages [90].
Advances in genomics: It’s currently more important than ever that more molecular markers, particularly SNPs identified through NGS platforms since this would expedite genomic breeding for weevil resistance and other key traits in Uganda. This has been enabled by recent research advances such as the published genome sequence of diploid I. trifida, the closest relative and putative progenitor of sweetpotato [71] . Ultimately, the completion of the ongoing whole genome sequencing of cultivated hexaploid sweetpotato in the near future will further enable maximum exploitation of genomics-assisted improvement of this crop in Uganda and the region.
Exploring the potential of heterosis based breeding: In the past, sweetpotato breeding mainly relied on the ability of breeders to identify parental genotypes possessing desirable traits, and to combine these parents through hybridization schemes such as the polycross and controlled cross nurseries [48,91,92]. Preliminary studies have however shown that there are better genetic gains from heterosis based breeding compared to using the polycross [92]. Nonetheless, the potential limitation of this approach is the high level of self and cross-incompatibilities in some of the diverse parental genotypes [93] in addition to seed set abortions.
The application of molecular approaches is critical for exploiting heterosis for sweetpotato improvement. Genetic markers SNPs will be critical for diversity analysis among parental genotypes and selection of diverse parents in constituting heterotic groups for use in population improvement [94-95]. Because of self-incompatibility and severe inbreeding depression in sweetpotato, heterotic groups are currently separated based on the long-term geographic adaptations of breeding parental genotypes such as the African, Asian, and South and North American heterotic groups [48]. The application of heterosis based breeding, through selecting and genotyping the best performing SPW resistant clones and subsequently utilizing the diverse and superior parents for the next cycle of population improvement, would minimize chances of recombining closely related parents, eventually leading to higher genetic gains.

14. Conclusions

Host plant resistance is the most effective approach for sweetpotato weevil management but to date, the development of sweetpotato weevil resistant varieties has not been so successful in Uganda. Nevertheless, some progress has been made in the past decades in the development of moderately resistant varieties being produced by the farmers in Uganda and the region. The underlying genetic and bio-chemical basis for resistance has been understood to some extent and molecular markers such as SNPs have been developed still not being fully utilized in breeding. More effort will be needed by sweetpotato breeders to develop more markers for mapping sweetpotato weevil resistance to facilitate marker assisted selection and genomic selection. With the on-going sequencing of the hexaploid sweetpotato genome, we anticipate that genomics-assisted breeding for sweetpotato weevil resistance will be expedited in the coming years. Further, the advances in sweetpotato phenomics and biochemistry globally will eventually pave way for the use of novel approaches for future improvement of sweetpotato for weevil resistance with resultant accelerated genetic gains for this trait in Uganda and the SSA region.

Author Contributions

Conceptualization, I.M. and B.Y.; writing—original draft preparation, I.M.; P.M., writing—review and editing, I.M., B.Y., D.M.C., B.M.O., R.T.S., M.A.O., F.O and A.K., project administration, B.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Bill & Melinda Gates Foundation (BMGF) through the PEARL I: Biochemistry-Based Selection and Development of Nutrient Rich, Weevil Resistant Sweetpotato Varieties in Uganda Sweetpotato project (Contract ID: OPP1112515).

Data Availability Statement

The raw data sets of the reviewed papers in this article are available for public and can be accessed online at: https://sweetpotatobase.org/.

Acknowledgments

The authors thank all the partners that have worked over the years in sweetpotato improvement in Uganda and SSA; International Potato Center (CIP), North Carolina State University (NCSU), and the National Crops Resources Research Institute for their contribution to the research reviewed in this paper.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Developmental stages of sweetpotato weevils, Cylas puncticollis (A-egg; B-larvae; C-pupa; D-adult) and Cylas brunneus (E-egg; F-larvae; G-pupa; H-adult).
Figure 1. Developmental stages of sweetpotato weevils, Cylas puncticollis (A-egg; B-larvae; C-pupa; D-adult) and Cylas brunneus (E-egg; F-larvae; G-pupa; H-adult).
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Figure 2. Sweetpotato storage roots shortly after harvest: A- Clean (no weevil damage); B-Weevil infested (visible damage).
Figure 2. Sweetpotato storage roots shortly after harvest: A- Clean (no weevil damage); B-Weevil infested (visible damage).
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Table 1. A comparison between Cylas puncticollis and Cylas brunneus [12,13,18,25].
Table 1. A comparison between Cylas puncticollis and Cylas brunneus [12,13,18,25].
Trait Cylas puncticollis Cylas brunneus
Morphology Eggs:0.45 x 0.30 mm in size
Larvae:5–10 mm long
Pupae:6–7 mm long; creamy-white cuticle
Adults: 5–8 mm long; eyes narrowly separated 		0.7 X 0.5 mm in size
7–8 mm in length
4–5 mm long; white in colour
5–7 mm long; eyes widely separated
Oviposition Females take 2–24 days before laying eggs Females start laying eggs a day or so after becoming sexually active
Development Takes place between 17.5°–35°C Is possible between 17.5°–32°C
Coloration Initially creamy white, but later change to gray and black Turn from creamy white to brown and finally black, some are bi-colored (brown and black)
Host range Has a wider host range including morning glory, cotton, sesame and maize Has a smaller host range including morning glory and water spinach
Distribution Reported in 24 African countries Recorded in 9 African countries
Dispersion Adults can fly for longer distances (up to 1000m) Adults fly for short distances (up to 80m)
Table 2. An overview of the management and control strategies for Cylas species.
Table 2. An overview of the management and control strategies for Cylas species.
Cultural practices
Use of clean planting material, crop rotation [29], hilling up and mulching, removal of alternate crops and wild plants, field sanitation [27,30], use of barrier crops, intercropping, planting of new crop away from weevil-infested fields, timely or early planting and harvesting before onset of the dry season [24,31], and flooding [32]
Chemical practices
Insecticides as foliar sprays controls weevils to some extent [33,34]. They can reduce the populations of adult weevils, but may not adequately control immature larvae due to their cryptic nature or when they have already infested roots and vines [8]. Dipping plant material into a synthetic pesticide before planting, can delay pest infestation for several months [27]. Insecticides are expensive and at times inaccessible to growers in SSA making their use impractical and unsustainable[35]
Biological
Natural enemies such as ants, maggots and wasps attack weevils, but most of them seem to be ineffective at suppressing SPW populations under field conditions [25,36]. Entomopathogenic fungi such as Beauveria bassiana have successfully been used to control SPWs in combination with other control methods. They caused a reduction in feeding ability, fecundity and egg viability in C. puncticollis [37]. Entomopathogenic nematodes such as Steinernema carpocapsae and Heterorhabditis bacteriophora, have shown potential for practical biological suppression of Cylas spp but are not readily available and small-scale farmers may not have the required purchasing power [21,38]. Bacteria such as Bacillus thuringiensis Berliner (Bt), have been developed to confer inherent pest resistance against SPWs [39,40]. Bt sweetpotato events against SPWs have been tested in SSA [7].
Host Plant Resistance
Involves the use of sweetpotato weevil resistant or tolerant clones [15,41]. Deep-rooting and early maturing varieties are less susceptible to infestation than shallow rooting and late maturing varieties [42].Efforts to develop SPW resistant cultivars are still ongoing in SSA
Transgenic sweetpotato plants expressing the Bt cry genes are also currently in use in some countries [43].
Table 3. Reaction of sweetpotato varieties released in Uganda to Cylas spp.
Table 3. Reaction of sweetpotato varieties released in Uganda to Cylas spp.
Year of release Variety Reaction to SPW
1995 “Bwanjule” MR
“New Kawogo” MR
“Sowola” MR
“Tanzania” S
“Wagabolige” MR
“Tororo 3” MR
1999 NASPOT 1 S
NASPOT 2 S
NASPOT 3 MR
NASPOT 4 MR
NASPOT 5 MR
NASPOT 6 MR
2004 “Ejumula” S
SPK004 (Kakamega) S
2007 NASPOT 7 S
NASPOT 8 S
NASPOT 9 O S
NASPOT 10 O S
“Dimbuka Bukulula” S
2010 NASPOT 11 S
2013 NASPOT 12 O S
NASPOT 13 O S
2017 NAROSPOT 1 MR
NAROSPOT 2 Low
NAROSPOT 3 Low
NAROSPOT 4 Low
NAROSPOT 5 Low
2023 NAROSPOT 6 MR
NAROSPOT 7 O MR
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