Modelling and manipulation of plant-aphid interactions: A new avenue for sustainable disease management of an important crop in Africa

Lead Research Organisation: Int Livestock Research Institute
Department Name: Biosciences Eastern and Central Africa

Abstract

In Eastern and Central Africa beans are a vital crop because they enrich the soil with fixed nitrogen (an indispensable natural fertilizer), which in turn supports the cultivation of other important crops such as corn (maize) and cassava. Beans are an essential part of the regional diet because they are rich in protein and crucially important micronutrients like iron and zinc. Since beans are predominantly grown and traded by women, this crop provides additional direct economic benefits to women and their children. Unfortunately, a number of viruses attack bean plants, causing severe crop losses from disease. Although there are a few bean varieties with resistance to one of these viruses (called bean common mosaic virus), a closely related virus that occurs widely in, and is indigenous to, Africa (bean common necrotic mosaic virus) causes plants of these 'resistant' lines to die. Thus, it is important to develop new strategies to defend this vital crop.


Our approach is to attack the insects (aphids) that transmit these viruses from plant to plant. We have found that aphid-plant interactions are controlled in large part by the plant's 'small RNA pathways'. Small RNA pathways are a recently discovered regulatory system used by plants and many other organisms to control the expression of their own genes as well as to fight off disease. The discovery of small RNA pathways has revolutionized biology and medicine. In plants, small RNA pathways control, among other things, the production of natural signal chemicals that attract or repel insect pests, including aphids. Intriguingly, viruses produce factors called 'silencing suppressors' that modify small RNA pathways. We have found that silencing suppressors affect the interactions of virus-infected plants with aphids in a way that is likely to enhance the rate at which these insects acquire viruses and transport them to other plants. We have assembled a team of scientists based in Uganda, Kenya and at two centres in the UK to translate these findings from the laboratory to the field and exploit them for protection of beans. However, aphids and the viruses they transmit are problems for all major crops and the work will yield vital data for the wider field of crop protection.

Our multinational team will collaborate to:

A. Identify potential factors involved in mediating plant-aphid communication in plants: small RNAs, the genes they control, and the chemical signals whose production they regulate.

B. Use the modelling methods provided by the discipline of mathematical epidemiology to help us design experiments (under lab and later field conditions) to predict how altering the attractiveness of plants (whether engendered by changes in the plant or deployment of signal chemicals as traps or decoys) could be used to help minimize or prevent the transmission of viruses.

C. Utilize the work from 1 and 2 to design experiments to test the effects on virus transmission of modifying plant responses to aphids or utilization of purified signal chemicals to trap or deter aphids under controlled and simulated field conditions.

D. To achieve impact by disseminating information gained from our work to African crop scientists, growers and consumers through the Pan-Africa Bean Research Alliance, a network of the national bean research programmes of 28 African nations.

Technical Summary

Our overall objective is to assess potential risks/benefits for disease management (using epidemiological modelling with experimental validation) from identifying and adapting the knowledge/tools (including gene sequences/semiochemicals/epidemiological models) from studying viral suppressor of RNA silencing-mediated effects on aphid-plant relations to develop 'push-pull'-type systems to protect bean. However, aphids are important pests and disease vectors affecting all major crops, meaning our results will have wide applicability. Our collaboration will translate work from model systems (Arabidopsis and tobacco) to a vital crop (bean) with uniquely African viral disease problems (with emphasis the combined effects of bean common mosaic virus and bean common necrotic mosaic). Key objectives/activities are listed with lead researcher(s) and time-scales indicated in parentheses.

1. Epidemiological modelling (Yrs 1-4, CAG, Cam)
2. Validation and exploration of modelling predictions in controlled conditions (Yrs 1-4, Cam)
3. Field surveys and data collection in Uganda (Yr. 1) and experiments utilizing data from 1 and 2, and field samples (Yrs. 2-4)(MA, CIAT)
4. Analyzing the effects of silencing suppressors on bean mRNA and small RNA profiles (Yrs 2-4) (JH, AD, BecA; DB, Cam)
5. Metabolite analyses to identify semiochemicals produced by bean that influence plant-aphid interactions (Yrs 2-4, Rothamsted)
6. Initiating pathways to impact activities via the Pan-Africa Bean Research Alliance, a network of the national bean research programmes of 28 African nations (Yr3/4; Lead: MA, CIAT).

Planned Impact

The project focuses on development of solutions to problems caused by viruses and the aphids that transmit them in bean. Bean (Phaseolus vulgaris) is an important crop because: it is a primary source of protein and trace elements in the East and Central African diet; it is a vital intercrop required for high yields and biotic and abiotic stress resistance in other crops including maize and cassava, and because it is of particular economic as well as nutritive value to women and children in the region. But the project will generate outputs (epidemiological models, genes, and gene sequences, and semiochemicals) that will be useful for addressing aphid and virus problems in any crop in any region, especially in the face of the treat to food security posed by spread of insecticide resistance, and the emergence of novel aphid-vectored diseases. Impact will be achieved through four interrelated activities.

1. Impact through Capacity Building The project enables BecA and ECABREN to expand research beyond their respective ILRI and CIAT core-funded activities but in line with priorities developed in consultation with African national partners both in the public and private sectors (see Letters of Support from NARO, Uganda and FICA Seeds Ltd., Uganda). Impact will be achieved through training of personnel at all levels especially the training of a PhD student and the Kenya and Uganda-based PDRAs in state-of-the-art methodologies. The project will also enhance the ability fo UK partners to contribute to future North-South collaborative projects.

2. Impact through Publication and Dissemination of Scientific Results including novel epidemiological models, transcriptomic and metabolomic datasets and semiochemicals, peer-reviewed papers and conference presentations.

3. Achieving Impact with Growers, National Research Organizations (NAROs), and Industry in the African arena utilizing the Pan Africa Bean Research Alliance's excellent network to feed information/tools to end-users (primarily small-holder growers including a high proportion of women). PABRA has a strong track record for participatory monitoring and evaluation in assessment of impact using results-based indicators to track project achievements and progress towards positive economic and social goals.

4. Achieving Impact: Public communication and engagement in the UK by engagement with the public through existing arrangements at Cambridge and Rothamsted Research.

Publications

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