How resistant plant varieties avoid suppression of RNA silencing by viruses as exemplified by sweetpotato: Better food security through virus control

Lead Research Organisation: University of Greenwich
Department Name: Natural Resources Institute

Abstract

Vegetatively-propagated crops are major staple foods in many developing countries, particularly in Africa where they provide about half of plant-derived dietary calories. Systemic viral infections are a main cause of yield loss in vegetatively-propagated crops as cutting etc taken from infected plants also are infected. By introducing inoculum at the very beginning of cropping cycles, infection spirals up rapidly and varieties can become completely infected (degenerated). In developed countries, certified virus-free schemes protect commercial cultivars of, for example, potato but are not commercially viable for staple food crops in small-scale, low-input, developing country farming systems. Here, the main control is through cultivars in which there is no or only slow degeneration so it can be controlled by careful selection of planting material. Absence of degeneration has been associated with an active defence mechanism found in all plants based on the generation of very short RNA particles which bind to single stranded RNA of plant viruses, destroying the target RNA and disrupting vital biological processes, notably replication. Hallmarks of this mechanism include initial symptoms becoming less severe, disappearing completely (recovery) and cuttings taken from such plants being free of infection (reversion). These are, for example, all present in the response of African sweetpotato landraces to infection with Sweet potato feathery mottle virus (SPFMV), the commonest virus of sweetpotato in Africa and worldwide and in the resistant cassava varieties currently at the frontline combating the cassava mosaic disease pandemic engulfing East and Central Africa. Molecular evidence supports virus resistance in sweetpotato being RNA silencing (RS)-based: in Africa, the main disease of the crop is sweet potato virus disease (SPVD) in which uncontrolled multiplication of SPFMV occurring when Sweet potato chlorotic stunt virus (SPCSV) co-infects is thought to be caused through two proteins, p22 and its own RNase3, encoded by SPCSV. Experiments have shown these proteins suppress host plant RS-based resistance, presumably 'freeing' co-infecting SPFMV from the control of RS-based resistance and allowing it to multiply and cause SPVD. In addition to our knowledge of how SPCSV aids SPFMV, diverse sweetpotato germplasm in Africa and at the International Potato Center based in the Americas where sweetpotato was originally domesticated includes landraces with natural extreme resistance to both SPFMV and SPCSV, with resistance to SPVD and plants engineered to silence SPFMV and SPCSV. By use of these, the project investigates how RS resistance normally controls a virus (SPFMV) and how to prevent its suppression, e.g., by SPCSV, and prevent degeneration. In this, it will rely on the molecular skills and facilities of the Sainsbury Laboratory, a world leader in RS-based resistance. Sweetpotato, as a major staple food crop in Africa and subject to viral degeneration including very damaging attack by SPVD, is already the target of breeding programmes and, even without fully understanding the mechanism of RS-based resistance in sweetpotato, the Ugandan Sweetpotato Program provides the lead in the region for developing superior virus-resistant varieties. Its close involvement in the project will enable improved resistant varieties to be deployed rapidly through the use of new sources of resistance, molecular identifiers of RS-based resistance, and understanding how to combat viral suppression of RS-based resistance. Participatory breeding approaches will ensure farmers' needs are addressed. As well as providing more food, especially for poor people, rapid deployment of resistant orange-fleshed sweetpotato varieties is essential for combating the widespread vitamin A deficiency in African children. Involvement of Uganda's Makerere University will also enable this knowledge to be deployed over a broader range of African food crops.

Technical Summary

RNA silencing (RS) is a fundamental plant defence involving small interfering RNA; RS-based resistance is achieved only when viral suppression is avoided. Sweet potato feathery mottle virus (SPFMV), the commonest virus of sweetpotato, induces only transient mild symptoms and associated reversion to healthy, hallmarks of RS defence, provides an alternative to certified virus-free schemes in low-input, developing country farming systems for sweetpotato and other vegetatively-propagated crops, e.g., cassava mosaic-resistant cassava. Sweetpotato virus disease (SPVD), the main disease of sweetpotato in Africa, involves both Sweet potato chlorotic stunt virus (SPCSV) and SPFMV. During co-infection, SPFMV increases in titre, often by several orders of magnitude and apparently in all tissues. SPCSV and SPFMV have already been sequenced. SPCSV has two RNA molecules: two proteins encoded by its RNA 1, p22 and an RNase3 have together been shown to suppress RS, providing a mechanism whereby SPCSV co-infection releases SPFMV from RS-based resistance and causes SPVD. How plants resist viruses through RS will be investigated by studying the known RS system in sweetpotato against SPFMV both in circumstance where resistant sweetpotato resist SPFMV when infecting alone and where it breaks down when co-infecting SPCSV suppresses RS. Diverse germplasm including extreme resistance to SPCSV and SPFMV now identified in CIP's worldwide sweetpotato collection, SPVD-tolerant African landraces and engineered resistance provide additional research entry points. Sweetpotato is a vital food and nutritional crop in many developing, especially African countries; partners include an African (Uganda) national breeding programme and university. The range and durability of SPFMV RS-based plant resistance, combining ability with other forms of resistance and molecular markers of resistance will be assessed, aiming to achieve rapid deployment of superior resistant varieties and sustainable control

Publications

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Description The research has demonstrated that certain sweetpotato varieties have an enhanced ability to revert to healthy and this is associated with an RNA silencing mechanism
Exploitation Route The most obvious way is through improved breeding for virus resistance
Sectors Agriculture, Food and Drink

 
Description The work is gradually changing the way agriculturalists in East Africa are maintaining sweet potato varieties and breeding new ones. The work has been published in moderate impact journals. The Bill & Melinda Gates Foundation has provided an award to a team member to continue the research which is continuing to support original findings
First Year Of Impact 2013
Sector Agriculture, Food and Drink
Impact Types Economic

 
Description Reversion
Geographic Reach Africa 
Policy Influence Type Participation in a national consultation
 
Description PEARL award
Amount $468,000 (USD)
Organisation Bill and Melinda Gates Foundation 
Sector Charity/Non Profit
Country United States
Start 08/2014 
End 08/2017
 
Description Makerere 
Organisation Makerere University
Country Uganda 
Sector Academic/University 
PI Contribution I am mentoring a staff member who was a PhD student on the original grant. I am helping make mainly research suggestions. I also helped with winning the award
Collaborator Contribution My partners are extending the value of our original research on the BBSRC-funded award
Impact The new project has only just been funded
Start Year 2014
 
Description RTB 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? Yes
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact I prepared two review documents and attended associated meetings

The RTB groups designed an appropriate way forward
Year(s) Of Engagement Activity 2013,2014