Targeting virus transmission in a vital crop for African food security

Lead Research Organisation: University of Cambridge
Department Name: Plant Sciences

Abstract

In East and Central Africa beans are a vital crop that naturally enriches the soil with nitrogen, providing natural fertilizer for other important crops such as maize and cassava. In the regional diet beans are important because they are rich in protein and critically important micronutrients. Since beans are mostly grown and traded by women, this crop provides important direct economic benefits to families & children. Unfortunately, a number of viruses attack bean plants, causing severe crop losses from disease.

Although some bean varieties have resistance to one of these viruses, bean common mosaic virus, a closely related virus that occurs widely in sub-Saharan Africa (bean common necrotic mosaic virus) causes plants of these 'resistant' lines to die. Thus, many farmers prefer to plant susceptible bean lines despite the risk of crop loss and it is important to develop new strategies to defend this vital crop.

The viruses are transmitted on the needle-like mouthparts of aphids. Importantly, the virus particles are lost by the aphid as soon as it feeds on a healthy plant; a weak link in the infection chain that we can exploit. Aphids are attracted to volatile chemicals released by plants. Virus infection can change these plants 'odours' so that aphids are encouraged to land on infected plants, acquire virus particles and then transport them to healthy plants. However, some bean varieties emit odours that are more attractive to aphids even when the plants are healthy. This means that if we plant mixtures of bean plants that include 'attractive' varieties we could decoy aphids away from the rest of the crop and slow disease transmission.

Even better, if we can decoy virus-bearing aphids to land on plants that are resistant to the virus, then as soon as the aphid feeds it will lose the virus particles. This would effectively 'sanitize' the aphids and stop them spreading the virus, as well as dumping the virus into plants in which it cannot grow. An additional benefit of using a mixture containing a limited number of resistant plants is that viruses will be under less pressure to evolve new strains that can overcome resistance and, in cases where virus infection kills resistant plants, only a small proportion of the crop will be lost. Since aphids and related insects transmit the majority of plant viruses the method could be applied to a wide range of crops.

Experiments under controlled conditions using varieties of a plant called Arabidopsis and an aphid transmitted virus called cucumber mosaic virus showed that aphid and virus spread can be altered using combinations of plants with different levels of attractiveness to aphids. A pilot field experiment in Uganda using mixtures of bean varieties with different degrees of attractiveness to aphids showed that aphids can be detained on more attractive varieties and inhibited from moving to other plants until close to harvest time, showing that our approach can work under farm conditions.

Our multinational team will:

A. Screen bean varieties that are popular in bean-growing regions in Kenya & Rwanda with respect to their attractiveness to aphids. We will identify the chemical odours emitted by plants that are most attractive to aphids. It is important to work with local varieties since farmers prefer certain bean types for hardiness under local conditions, cooking properties and local marketability. We will focus particularly on identifying aphid-attractive varieties carrying one or more virus resistance genes.

B. Mathematically model the consequences of different arrangements and mixtures of attractive/repellent/susceptible/resistant plant lines on aphid and virus spread in fields. This will not only help us design our field and lab experiments but also to analyze the data we obtain.

C. Test our models and lab experiments in Kenya & Rwanda to devise the most effective & practical field designs that minimize crop losses due to viral diseases.

Technical Summary

We will devise methods to make better use of existing limited, genetically-determined virus resistance in common bean by creating scenarios in which aphids are lured to settle on plants with resistance to the bean-infecting viruses most prevalent in East & Central Africa i.e. BCMV and BCMNV. For non-persistently transmitted viruses (including these viruses) viral particles detach from aphid mouthparts as soon as aphids feed. 'Pulling' aphids towards resistant plants will limit virus spread since aphids subsequently migrating away from these decoys will no longer carry infection. We will devise field designs using mixtures consisting predominantly of farmer-preferred varieties (which typically are BCMV/BCMNV susceptible) protected by inclusion of aphid-attractive, resistant lines. We reason that this is a sustainable approach to protection against pathogens that have a propensity to evolve resistance-breakage and/or when deployment of 100% resistant plants is inadvisable due to problems with resistance (e.g. black-root disease).
The programme comprises three work packages:
A. Identify Kenyan and Rwandan farmer-preferred common bean varieties and virus-resistant CIAT lines that can be used in field designs. We will use a combination of aphid choice and feeding assays at Cambridge and analysis of headspace volatiles by GC-MS and electroantennagram analysis at Rothamsted.
B. Mathematically model the spread of non-persistently transmitted viruses in mixtures. This process will be iterative, using field data (from Kenya and Rwanda) and experiments with beans under controlled conditions to improve and refine models.
C. Validate models under controlled conditions and in field experiments in Kenya and Rwanda. This will be done with project partners with capabilities to monitor aphid distribution, virus infection and yield over four growing seasons in three locations in Kenya (BecA-ILRI campus and KALRO centres at Kiboko & Mugaga) & Rwanda at RAB, Kigali.

Planned Impact

The project builds on work by the collaborators on the effects of virus infection on interactions between common bean & aphids (esp. Aphis fabae, Myzus persicae). Outputs of this work include findings that infection of common bean remodels host gene expression, inhibits prolonged aphid feeding, and alters emission of aphid-perceivable plant volatiles. Collectively, these effects enhance aphid-mediated transmission of non-persistently transmitted viruses (incl. the most important: bean common and bean common mosaic necrosis virus) to new hosts. Modelling indicates that decoying virus-bearing aphids to attractive plants will inhibit virus dissemination- born out by experiments under controlled conditions (using mixed Arabidopsis accessions, cucumber mosaic virus & M. persicae) & in the field by tracking aphid movement through bean mixtures. We hypothesize that including aphid-attractive, resistant plants in mixtures will decrease the proportion of aphids carrying viruses and thus decrease the basic reproduction number R0 to >1, inhibiting disease spread.

Translating this research & its outputs (incl. field designs, seed mix combinations, epidemiological models, semiochemicals) is vital for addressing problems posed by non-persistently transmitted viruses in many crops & in particular where food security is further threatened by spread of insecticide resistance within aphid populations or where access to chemical inputs is limited, where novel aphid-vectored diseases are emerging or where genetic resistance may be limited in its effectiveness. However, the approach's impact would be particularly important for common bean cultivation by resource-limited smallholder farmers in East and Central Africa, in which mixed cropping is the norm; indeed, bean is a vital intercrop required for high yields (via N fixation) and biotic and abiotic stress resistance in other crops (incl. maize, cassava, banana). Bean is an important source of protein & trace elements in the East and Central African diet and is of critical economic as well as nutritive value to women & children in the region.

Impact will be achieved through three interrelated activities.

1. Impact through Capacity Building. Dr. Appolinaire Djikeng our sub-contract partner & BecA-ILRI via their unique collaborator network incl. alumni, Governments, Growers, National Research Organizations & Industry in East and Central Africa & via the CG system including CIAT's linkages with the Pan Africa Bean Research Alliance provides a clear pipeline for technology transfer & knowledge sharing to National Agricultural Research services (NARS), growers, breeders, seed companies and extension personnel to promote income generation and improved nutrition in the region. Monitoring, evaluation, impact assessment and delivery activity through national research partners & extension services is managed Helen Altshul, BecA's development partnerships specialist. At Rothamsted Professors Toby Bruce & John Pickett have unparalleled experience in translation of basic research to improvement of smallholder agriculture in Africa, most notably the push-pull system, through their close collaborations with scientists in Africa.

2. Impact through Publication and Dissemination of Scientific Results including novel epidemiological models and elucidation of mechanisms underpinning virus-plant-aphid interactions via peer-reviewed papers & conference presentations.

3. UK Public engagement will be through existing outreach activities at Cambridge & Rothamsted. For outputs with UK commercial potential pathways exists via Cambridge's Innovation & Enterprise Project Officer, Dr Mariana Fazenda via the CambPlants Industry Club a hub hosted linking institutes, SMEs & UK industry & at Rothamsted via the Knowledge Exchange & Commercialisation Office.

Publications

10 25 50
 
Description Work is still in progress but filed experiments have been established and are yielding valuable data for model parameterisation. Mathematical modelling has yielded key insights into the effects of plant attractiveness in mixed cropping. The experimental data currently being obtained will be used to confirm/refute model. Mixed cropping simulation under controlled conditions using model plants indicates that specific filed designs effectively inhibit aphid-mediated virus transmission.
Exploitation Route Once complete the work will be usable by agronomists and plant protection specialists for devising low input methods for inhibiting virus transmission by insect.
Sectors Agriculture, Food and Drink

 
Description Seeding Catalyst Award BB/SCA/Cambridge/17
Amount £18,284 (GBP)
Funding ID Seeding Catalyst Award is BB/SCA/Cambridge/17. Title of sub-project 'The Potential of Castor Bean Derived Natural Products as Plant Protection Agents' 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 10/2017 
End 02/2018
 
Description Collaboration with Scientists at KALRO Kenya 
Organisation Kenya Agriculture & Livestock Research Organization (KALRO)
Country Kenya 
Sector Private 
PI Contribution KALRO is providing field sites for experiments under the auspices of Award 'Targeting virus transmission in a vital crop for African food security'.
Collaborator Contribution KALRO scientists are providing field sites, expertise and personnel for testing of bean line mixtures to inhibit aphid-mediated virus transmission.
Impact Too early in the project to report.
Start Year 2017
 
Description Partnership with scientists in Rwanda 
Organisation Rwanda Agriculture Board
PI Contribution We have partnered with scientists at the Rwandan Agricultural Board to carry out field experiments on bean plant mixtures to disrupt the dynamics of aphid-mediated virus transmission. This is under the auspices of Award 'Targeting virus transmission in a vital crop for African food security'.
Collaborator Contribution Provision of fields, advice and personnel.
Impact In progress.
Start Year 2017
 
Description Reach & Teach Science in Africa Project - A capacity building programme to strengthen research and innovation in sub-Saharan Africa 
Organisation University of Abomey-Calavi
PI Contribution Building on previous successful workshops for African Scientists at Cambridge in collaboration with Dr Carol Ibe (Cambridge) (http://www.jrbiotekfoundation.org/summit_speakers/dr-john-carr/), Carr obtained GCRF Global Impact Acceleration Account (GIAA) funds to set up a 'pilot' project for a crop biotech workshop to be held in collaboration with the Laboratory of Genetics, Horticulture and Seed Science (GBioS) at the University of Abomey-Calavi in Benin Republic, West Africa from 25-29th March 2019. The named PDRA on 'Targeting virus transmission in a vital crop for African food security', Dr Trisna Tungadi, will also be an instructor. Details are in the text box below.
Collaborator Contribution The Reach & Teach Science in Africa project is based on exchange of scientific knowledge, research tools and innovative approaches to help African researchers and academics to contribute to agricultural productivity and food and nutrition security in sub-Saharan Africa. Our first collaborative partner for this project is the Laboratory of Genetics, Horticulture and Seed Sciences (GBioS), University of Abomey-Calavi, Benin Republic. GBioS is positioning itself to be by 2022, a leading Plant Genetic Resources and Horticultural Research Group of Excellence, recognized nationally, regionally and internationally for its quality, relevance and impact. With a strong focus on agricultural research, education and capacity building, GBioS is looking to i) unlock the potential of neglected crops, ii) improve agronomic practices, iii) improve access of smallholder farmers to quality seeds, and iv) provide high-quality training and research tools in molecular plant breeding and bioinformatics to 118 postgraduate students (20 PhD and 98 MSc students) currently involved in genetics and plant breeding programmes in DAC countries such as Benin, Niger, Burkina Faso, Nigeria, Ethiopia, Malawi, Zimbabwe and Cameroon. The students are looking to use molecular assisted tools and bioinformatics to develop better cultivars that will ultimately contribute to food security in their countries, hence an excellent opportunity for the Department of Plant Sciences, University of Cambridge to position itself as a leader and major contributor of knowledge, expertise and innovative approaches to support the next generation of African researchers and plant breeders.
Impact In progress - the workshop will be 25-29th March 2019. Training will have mid to long term capacity building impact on the ability of regional scientists to carry out research and teach.
Start Year 2019
 
Description Role of poleroviruses in maize lethal necrosis epidemics in Africa, a case study of Kenya 
Organisation Kenya Agriculture & Livestock Research Organization (KALRO)
Country Kenya 
Sector Private 
PI Contribution Experience gained on insect vector identification while working on 'Targeting virus transmission in a vital crop for African food security' and the previous SCPRID grant by the Cambridge UK (PI, Carr) group has enabled us to form a new collaboration with Drs Jane Waimatha and Paul Kuria to investigate the possible involvement of an aphid-transmitted polerovirus in the elicitation of a novel disease of maize in Kenya. The work is funded by the GCRF-CONNECTED Network (https://www.connectedvirus.net/). Details of the project are in the next text box.
Collaborator Contribution Maize, the most important cereal crop and dietary carbohydrate source in Kenya, is seriously threatened by maize lethal necrosis (MLN) disease, which causes crop losses of up to 100%. MLN results from double infection by Maize chlorotic mottle virus (MCMV) and (most typically) the potyvirus Sugar cane mosaic virus (SCMV). These viruses 'synergize' i.e. cause worse symptoms than either virus alone. The Co-Is discovered that MLN and a novel disease (atypical MLN: AMLN) may also be caused by synergy between MCMV and other viruses, including a polerovirus, Maize yellow dwarf virus-RMV (MYDV-RMV). MCMV is beetle-vectored but SCMV & MYDV-RMV are aphid-transmitted, but which insect species are the most important vectors is unknown. This presents a serious barrier to understanding MLN/AMLN epidemiology and improving disease control. The Co-Is also found that Kenyan SCMV strains are highly diverse, explaining the inadequacy of current diagnostics. Our three packages will create a platform for future work to identify, combat and eradicate MLN/AMLN. Work Package 1. We will determine definitively if MYDV-RMV synergizes with MCMV using next-generation sequencing to identify viruses in plants with MLN/AMLN, and by recreating mixed infections under controlled conditions. Work Package 2. We will identify vector species transmitting MLN/AMLN-associated viruses by DNA barcoding and use next-generation sequencing to identify viruses carried by potential vectors present in MLN/AMLN-affected fields in Kenya. Work Package 3. We will utilize the Co-I's single nucleotide polymorphism and polyprotein sequence analyses to improve diagnostics for the three distinct groups of SCMV in Kenya. This is vitally important throughout sub-Saharan Africa for tracking MLN and to aid breeders in development of MLN/SCMV-resistant maize lines. Achieving Impact. Using KALRO's plant health outreach network and media contacts, key information on MLN diagnosis and control will be disseminated to Kenyan farmers, consumers and policymakers.
Impact The work is currently in progress. So far there has been a visit by Carr (UK PI) to KALRO and field sites to provide training in capture/sampling of insect viral vectors and preparation of material for sequencing and viral metagenomics.
Start Year 2018