Viral metagenomics of aphids present in bean and maize plots on mixed-use farms in Kenya reveals the presence of three dicistroviruses including a novel Big Sioux River virus-like dicistrovirus

Background: Aphids are major vectors of plant viruses. Common bean (Phaseolus vulgaris L.) and maize (Zea mays L.) are important crops that are vulnerable to aphid herbivory and aphid-transmitted viruses. In East and Central Africa, common bean is frequently intercropped by smallholder farmers to provide fixed nitrogen for cultivation of starch crops such as maize. We used a PCR-based technique to identify aphids prevalent in smallholder bean farms and next generation sequencing shotgun metagenomics to examine the diversity of viruses present in aphids and in maize leaf samples. Samples were collected from farms in Kenya in a range of agro-ecological zones. Results: Cytochrome oxidase 1 (CO1) gene sequencing showed that Aphis fabae was the sole aphid species present in bean plots in the farms visited. Sequencing of total RNA from aphids using the Illumina platform detected three dicistroviruses. Maize leaf RNA was also analysed. Identification of Aphid lethal paralysis virus (ALPV), Rhopalosiphum padi virus (RhPV), and a novel Big Sioux River virus (BSRV)-like dicistrovirus in aphid and maize samples was confirmed using reverse transcription-polymerase chain reactions and sequencing of amplified DNA products. Phylogenetic, nucleotide and protein sequence analyses of eight ALPV genomes revealed evidence of intra-species recombination, with the data suggesting there may be two ALPV lineages. Analysis of BSRV-like virus genomic RNA sequences revealed features that are consistent with other dicistroviruses and that it is phylogenetically closely related to dicistroviruses of the genus Cripavirus.Work was funded by a grant from the Sustainable Crop Production Research for International Development programme funded by the UK Biotechnology and Biological Sciences Research Council (BBSRC) with co-funding from the UK Department for International Development, the Bill & Melinda Gates Foundation, the Department of Biotechnology of India’s Ministry of Science and Technology, and the Indian Council of Agricultural Research (BB/J011762/1) and a Global Challenges Research Fund Foundation Award (BB/P023223/1). LAB was funded by a Cambridge BBSRC doctoral training programme studentship

Three Aphid-Transmitted Viruses Encourage Vector Migration From Infected Common Bean (Phaseolus vulgaris) Plants Through a Combination of Volatile and Surface Cues

Bean common mosaic virus (BCMV), bean common mosaic necrosis virus (BCMNV), and cucumber mosaic virus (CMV) are important pathogens of common bean (Phaseolus vulgaris), a crop vital for food security in sub-Saharan Africa. These viruses are vectored by aphids non-persistently, with virions bound loosely to stylet receptors. These viruses also manipulate aphid-mediated transmission by altering host properties. Virus-induced effects on host-aphid interactions were investigated using choice test (migration) assays, olfactometry, and analysis of insect-perceivable volatile organic compounds (VOCs) using gas chromatography (GC)-coupled mass spectrometry, and GC-coupled electroantennography. When allowed to choose freely between infected and uninfected plants, aphids of the legume specialist species Aphis fabae, and of the generalist species Myzus persicae, were repelled by plants infected with BCMV, BCMNV, or CMV. However, in olfactometer experiments with A. fabae, only the VOCs emitted by BCMNV-infected plants repelled aphids. Although BCMV, BCMNV, and CMV each induced distinctive changes in emission of aphid-perceivable volatiles, all three suppressed emission of an attractant sesquiterpene, α-copaene, suggesting these three different viruses promote migration of virus-bearing aphids in a similar fashion

Susceptibility of five cabbage varieties to attack by aphids (Hemiptera: Aphididae) in the Accra plains of Ghana

We investigated the susceptibility of five cabbage varieties (‘Oxylus’, ‘Super Cross’, ‘Vantar F1 Hybrid’, ‘Santa’F1 and ‘Fortune’) to aphids. Trials were set up in the Accra plains for two rainy seasons in 2017. The first trial examined aphids’ infestation and the second included weekly blanket spray of neem oil at 0.48 L/ha (60ml/15L water) during the second rainy season. Five systematically sampled cabbage leaves per plot were examined for the numbers of aphids and associated natural enemies (predators). Symptoms of aphid attack (incidence and severity of infestation) were also recorded. Lipaphis erysimi pseudobrassicae (Davis) and Myzus persicae (Sulzer) (Hemiptera: Aphididae) were the two aphid species observed and their numbers differed significantly between varieties in both seasons during the first but not the second trial. Few aphids settled on ‘Oxylus’, while more occurred on ‘Fortune’. L. e. pseudobrassicae was the most abundant aphid on all the varieties. Aphid numbers were significantly decreased by neem application. Occurrence of natural enemies did not differ significantly between varieties, except for spiders during the major rainy season. There was no significant difference in aphid infestation between varieties during the first season as all of them completely succumbed to the infestation, while in the second season aphid incidence and severity of infestation was highest on ‘Fortune’, with ‘Oxylus’ being the least attacked by aphids. The crop yield was zero during the first season without protection for all the varieties. However, in the second season, lower yields (0.19-3.66 t/ha) was obtained with cabbage without protection, and much higher yields (14.8-21.1 t/ha) were obtained on neem-treated plots.This work was funded by grants to KOF and JPC from Cambridge-Africa Partnership for Research Excellence (CAPREx), the ALBORADA Trust, the UK Biotechnological and Biological Research Council (BBSRC) Global Challenges Research Fund (GCRF) Impact Acceleration Account (BB/GCRF-IAA/04) and the BBSRC CONNECTED Network (BB/R005397/1: https://www.connectedvirus.net/). FOW was supported by a grant to JPC from the BBSRC SCPRID scheme (BB/J011762/1) and by a Royal Society-FLAIR Fellowship (Grant number FLR\R1\190462)

First Report and Distribution of the Indian Mustard Aphid, Lipaphis erysimi pseudobrassicae (Hemiptera: Aphididae) on Cabbage (Brassica oleracea var capitata) in Ghana.

The presence of large colonies of aphids is associated with a devastating novel necrotic disease of cabbage (Brassica oleracea var. capitata) in Ghana that is thought to be of viral etiology. In this study, we used molecular taxonomic tools to identify the aphid species present on these diseased cabbage plants. This was confirmed using two key features for morphological identification, involving the length of cornicles and shape of cauda for the wingless forms of the aphids. Two species of aphids were identified and their distribution in Ghana indicated. One was the generalist aphid Myzus persicae (Sulzer) (Hemiptera: Aphididae) but the most abundant was the brassica specialist aphid, Lipaphis erysimi pseudobrassicae (Davis) (Hemiptera: Aphididae), which is one of the most destructive pests of brassica crops in some countries in Africa and other parts of the world. L. erysimi has been reported in Benin, Mali, South Africa, India, China, and United States, but this is the first formal report of L. erysimi pseudobrassicae in Ghana. The correct identification of L. erysimi is crucial, suggesting that it has recently become one of the most common species of aphid found on cabbage plants in Ghana.This work was funded by grants to KOF and JPC from Cambridge-Africa Partnership for Research Excellence (CAPREx), the ALBORADA Trust, the UK Biotechnological and Biological Research Council (BBSRC) Global Challenges Research Fund (GCRF) Impact Acceleration Account (BB/GCRF-IAA/04) and the BBSRC CONNECTED Network (BB/R005397/1). FOW was supported by a grant to JPC from the BBSRC SCPRID scheme (BB/J011762/1) and by a Royal Society-FLAIR Fellowship (Grant number FLR\R1\190462). We also acknowledge all the farmers that cooperated during the survey

Differential effects of weather, plant phenology and predators on the seasonal variation of aphids on cabbage

The aphids Lipaphis erysimi pseudobrassicae (Davis) and Myzus persicae (Sulzer) pose serious threats to the production of cruciferous crops in the tropics. Understanding their population dynamics is important for developing integrated pest management programmes to minimize their damage to crops. This study investigated the effects of climatic factors, natural enemies and plant age on the population dynamics of these pests. The population density of aphids and their natural enemies in 20 cabbage plants, and weather conditions were monitored for five cropping seasons from 2019 to 2021 in two agroecological zones of Ghana (Coastal Savannah and Deciduous Forest zones). The highest population density of L. e pseudobrassicae was recorded in January (dry season) in both agroecological zones, while the highest population density for M. persicae occurred in September (minor rainy season) and August (dry spell) in the Coastal Savannah and Deciduous Forest zones, respectively. The highest aphid densities were noted to occur during periods with low relative humidity and low rainfall. The population density of L. e. pseudobrassicae was significantly negatively related to plant age, air temperature and relative humidity, and positively related to syrphids (Paragus borbonicus) and spiders in the Coastal Savannah zone, while in the Deciduous Forest zone it was significantly positively related to coccinellids. On the other hand, M. persicae population density was significantly positively related to syrphids and coccinellids in the Deciduous Forest zone. Rainfall negatively affected syrphids in the Coastal Savannah zone, while air temperature positively affected syrphids and negatively affected spiders in the Deciduous Forest zone. Coccinellids had a significant positive relationship with relative humidity in the Deciduous Forest zone. This study provides important insights into the key factors that regulate aphid population densities on cabbage and will support development of timely interventions to manage these pests.Funding was provided by the German Academic Exchange (DAAD) for the PhD studies of FEE, the BBSRC CONNECTED Network Grant (BB/R005397/1) to K.O.F and J.P.C

Differential effects of weather, plant phenology and predators on the seasonal variation of aphids on cabbage

The aphids Lipaphis erysimi pseudobrassicae (Davis) and Myzus persicae (Sulzer) pose serious threats to the production of cruciferous crops in the tropics. Understanding their population dynamics is important for developing integrated pest management programmes to minimize their damage to crops. This study investigated the effects of climatic factors, natural enemies and plant age on the population dynamics of these pests. The population density of aphids and their natural enemies in 20 cabbage plants, and weather conditions were monitored for five cropping seasons from 2019 to 2021 in two agroecological zones of Ghana (Coastal Savannah and Deciduous Forest zones). The highest population density of L. e pseudobrassicae was recorded in January (dry season) in both agroecological zones, while the highest population density for M. persicae occurred in September (minor rainy season) and August (dry spell) in the Coastal Savannah and Deciduous Forest zones, respectively. The highest aphid densities were noted to occur during periods with low relative humidity and low rainfall. The population density of L. e. pseudobrassicae was significantly negatively related to plant age, air temperature and relative humidity, and positively related to syrphids (Paragus borbonicus) and spiders in the Coastal Savannah zone, while in the Deciduous Forest zone it was significantly positively related to coccinellids. On the other hand, M. persicae population density was significantly positively related to syrphids and coccinellids in the Deciduous Forest zone. Rainfall negatively affected syrphids in the Coastal Savannah zone, while air temperature positively affected syrphids and negatively affected spiders in the Deciduous Forest zone. Coccinellids had a significant positive relationship with relative humidity in the Deciduous Forest zone. This study provides important insights into the key factors that regulate aphid population densities on cabbage and will support development of timely interventions to manage these pests.Funding was provided by the German Academic Exchange (DAAD) for the PhD studies of FEE, the BBSRC CONNECTED Network Grant (BB/R005397/1) to K.O.F and J.P.C