Advances in Virus Research: 46

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Mayo, J. Maniloff, U. Desselberger, and L. Ball, Eds. Ecological Entomology 30, Advances in Virus Research 65, Ecological Entomology 31, In: Encyclopedia of Virology Third edition. Van Regenmortel Eds. Neotropical Entomology 37, Current Topics in Microbiology and Immunology , Virologica Sinica 24, In: Insect Virology, Assgari, S. Caister Academic Press, UK. Gress, J. King, M. Adams, E. Carstens, E. Elsevier, San Diego, CA. Journal of General Virology 98, Published online: www.

Author's personal copy 16 Elizabeth A. Collected from a total of 84 papers. Even in regions where BCMV has been long established, there are reports of its occurrence in novel hosts and cultivation areas Li et al. However, BCMNV has occasionally been trans- ported to other parts of the world through contaminated bean seed Beaver et al. Both viruses are major constraints on bean production and can cause seri- ous crop losses Morales, Thus, the use of the I gene cultivars in bean cultivars in Central and Eastern Africa where BCMNV strains exist can be counterproductive leaving farmers with very few choices for controlling bean-infecting potyviruses see Section 8.

Potyviruses are the most economically destructive plant-infecting viruses in Australia Coutts et al. Australia are indigenous virus species not found elsewhere. Interestingly, these native potyviruses belong to one lineage of the BCMV group see Section 2 but tend to be found in native and naturalized wild plants rather than in cultivated plants Coutts et al. However, a recent study indicated that indigenous legume-infecting potyviruses can jump from native to introduced plants, which could conceivably pose a threat to cul- tivated plants in the future Kehoe et al.

Thus, when examining the earlier liter- ature, it should be remembered that before the reclassification, the host range of BCMNV was not considered separately from that of BCMV. The most notable cultivated legume hosts are Phaseolus species predomi- nately P.

These include Phaseolus vulgaris, Crotalaria incana, Rhynchosia sp. Thus, an outbreak can be triggered by the use of contaminated seed stock and amplified by aphid-mediated virus transmission to generate an epidemic Hampton, Alternatively, the viruses may infect a healthy crop population when viruliferous aphids immigrate from infected wild plants Sengooba et al.

This stability of virus in the embryo is likely a major contributory factor for seed being the most impor- tant route for long-distance worldwide dissemination of BCMV and BCMNV through trade. For example, it is believed that the BCMV epidemics in Europe and America were most likely initiated by seed stock contamination. Of the stock tested, two foundation seed lots of line UI produced in and and one foundation seed lot of UI 60 produced in were contaminated with the virus Forster et al. Perhaps not surprisingly, the bean crop in south-central and south-western Idaho was heavily affected by this contamination.

The percentage of infected seed varies from 0. This variability in infection rate is to some extent explained by the season and developmental stage of the plants at which a crop is exposed to infection.

Morales and Castano discovered that the incidence of seed transmis- sion of five BCMV strains in 14 mosaic-susceptible bean cultivars is signif- icantly affected by the inoculation date. Plants inoculated within the first 20 days of their vegetative period had a significant increase in the percentage of seed transmission. Most of the literature describing aphid-mediated transmis- sion of BCMV was published in the period — In , Halbert and colleagues studied the transmission of BCMV by five cereal aphids Diuraphis noxia, Metopholophium dirhodum, Rhopalosiphum padi, Schizaphis graminum, and Sitobion avenae as well as Myzus persicae Halbert et al.

They found that of all aphid species tested, only D. However, all aphids do not transmit all viruses with equal efficiency and aphid species-specific transmis- sion characteristics are likely to be important factors in viral epidemiology. In an investigation of the efficiency of various aphid species in transmit- ting CMV in bean, it was found that the bean specialist aphid Aphis fabae and a generalist aphid, Myzus persicae, were, in fact, poor vectors for this virus Gildow et al.

Similar tests have also been done to determine the transmission effi- ciency of aphid species in transmitting PVY to potato. It is important to carry out more of these types of experiment for a wider range of crop—vector—virus pathosystems for two reasons. First, because too much may be assumed from the presence of specialist aphids on infected plants about their role in transmitting viruses to crops; generalists and nonspecialists may be more potent vectors.

Second, in certain agricultural systems, for example in African smallholder farming, the intercropping of multiple plant species is common Mucheru-Muna et al. While having other benefits, intercropping may exacerbate aphid, and therefore vector, diversity and availability. But for successful aphid-mediated potyvirus transmission, the HC-Pro is essential. Author's personal copy 24 Elizabeth A. Hamid et al. Currently, the aphid receptor molecule s responsible for binding of potyvirus particles within the stylet have not been definitely identified.

There is growing evidence that these alterations may benefit viruses by, among other things, affecting the interactions of plants with insect vectors Jones, This can be due to changes in the emission of volatile compounds to make plants more or less attractive to potential vectors Mauck et al. This may also be the case for potyviruses. Boquel, Giordanengo, and Ameline observed that feeding behavior of the aphids Macrosiphum euphorbiae and Myzus persicae was affected differentially on potato plants infected with PVY, with feeding deterrence induced against the potato specialist Macrosiphum euphorbiae but resistance to feeding by Myzus persicae a polyphagous aphid was diminished.

The effects of potyviruses on plant—aphid interactions are conditioned by specific viral gene products. Aphid Myzus persicae performance was enhanced on plants of A. In these TuMV-infected plants, it was found that deposition of callose which has defensive properties against aphids was decreased and the levels of certain amino acids were elevated in the phloem sap and that these changes were attributable to the TuMV NIa-Pro Casteel et al. In contrast, Westwood et al. It can be seen that the effects of virus infection on aphid—plant inter- actions are complex, and it has been proposed that the same virus can have different effects on different hosts in order to promote transmission between some, while enhancing survival and reproduction of vectors on other hosts Westwood et al.

This complex set of relationships among hosts, vectors, and viruses may offer a new route to control virus infection reviewed by Bragard et al. Author's personal copy 26 Elizabeth A. In response, common bean cultivars have been specifically bred for genetic resistance to both viruses. Recessive resistance genes are available but they are virus strain-specific, and thus, it is difficult to breed bean cultivars that possess a broad resistance to many strains of BCMV and BCMNV based on one of these genes alone.

Therefore, some breeding efforts are focused on utilizing molecular markers to pyramid recessive genes such as bc-u, bc-1, bc, bc-2, bc and bc-3, with the dominant I gene in attempts to provide the broadest possible resistance Kelly et al. Bean genotypes carrying the bc-3 gene for BCMV resistance were found to carry homozy- gous nonsilent mutations at codons 53, 65, 76, and in a PveIF4E coding sequence and these mutations closely resembled a pattern of mutations determining potyvirus resistance in other plants Naderpour et al.

This indicates a high level of variability at the locus, perhaps driven by coevolution with bean-infecting potyviruses. In a similar develop- ment, transgenic plum Prunus domestica plants expressing a silencing construct directed against PdeIF iso 4E exhibited resistance to PPV, which causes the economically important Sharka disease in Prunus species plums, peaches, apricots, cherries, and related ornamentals Wang et al.

In the future, it may be possible to further refine the creation of artificial recessive resistance phenotypes using genome editing. This methodology, which produces mutations that are indistinguishable from those that can occur naturally, could be used to alter specific amino acid residues in eIF4- type translation factors rather than to downregulate entirely the expression of the gene encoding the factor.

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This would have the advantage of depriving a potyvirus of a cognate eIF4-type factor, while minimizing any negative effects on host plant fitness. As far as we are aware, no manipulation of viral host factors utilizing transformation with either conventional trans- formation technologies or genome editing has been attempted in bean. To the best of our knowledge, the I gene is yet to be cloned. This means that once the I gene has been isolated there will be considerable scope for altering its properties so as to expand its ability and make it effective against BCMNV. Farnham and Baulcombe created a mutant Rx gene RxM1 that, when expressed in transgenic plants, enabled them to respond to PopMV with a hypersensitive-like reaction.

However, this response was not sufficient to completely restrict PopMV and virus continued to spread, leading to sys- temic necrosis and host death. That is, both types of plant possess an R gene prod- uct that mediates a weak recognition of a virus. In more recent work from the same group, Harris et al. Expression of virus-derived gene sequences to in transgenic plants pathogen-derived resistance is a highly effective method of protection against viruses. Unfortunately, the application of technologies based on plant transfor- mation has been very slow in common bean; partly due to its relatively low efficiency for Agrobacterium tumefaciens-mediated transformation, which can be remedied by careful choice of A.

The only successful study of which we are aware in which a transgenic approach has been used in common bean to generate resistance to a virus is for the Begomovirus Bean golden mosaic virus BGMV Bonfim et al. From the data published so far, it is not clear how the transgene engenders resistance; although virus sequence-specific short-interfering RNA molecules were detected in the plants of EMBRAPA 5. A novel approach utilizing RNAi to obtain resistance without producing stably transformed plants exploits RNAi by the topical application of exog- enous, sequence-specific dsRNA Gan et al.

Cur- rently, there are limitations for the spray application of dsRNA for field use. However, a discussion of the technical aspects of this approach is beyond the scope of this chapter and readers are directed to Robinson et al. The aim is to validate these constructs for both transgenic and topical spray applications. Topical application will be aided by nanoparticle-based delivery of RNAi effector molecules in order to overcome the instability of dsRNA as well as to facilitate a controlled delivery at the leaf surface.

In any case, these chemicals are relatively expensive, rendering them impractical for use by many small- holder farmers in developing countries.

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Walkey and Dance found that the sprays diluted to 2. Work in this area has continued.

For example, recently Boquel et al. How- ever, it is unknown whether this method would be affordable or cost- effective for small-scale farmers. Investigation of how viruses themselves alter the emission of volatiles to aid in vectoring see Section 7. Application of these methodologies to bean will require improvements in transformation see Section 9. In the meantime, there is potential for utilizing plant extracts as homemade semiochemical-based aphid repellents by smallholder farmers Pickett et al.

Just as NBS-LRR immune receptors can trigger hypersensi- tive resistance following specific recognition of a pathogen effector mole- cule see Section 8 , there are also plant R genes known to or thought likely to encode NBS-LRRs that mediate recognition of and resistance to specific aphid species.

Plant virus vector interactions (Advances in Botanical Research Vol 36) : Rothamsted Research

Another interesting example is the tomato Mi-1 gene, which confers resistance to aphids Macrosiphum euphorbiae in leaf tissue and to nematodes in roots. Goggin et al. This may show how R gene trans- fer between even relatively closely related plants in this case, S. This approach was shown by Pitino et al. These workers showed that dsRNAs con- taining aphid sequence-specific sequences expressed in transgenic A.

Small but statistically significant decreases in the reproduc- tion of aphids placed on these plants were noted for lines expressing either of these constructs Pitino et al. Regrettably, however, because of the rapidity with which BCMV, BCMNV, and other nonpersistently transmitted viruses are injected by aphids into a healthy host or acquired by them from an infected plant, that neither this approach nor the use of natural aphid specific R genes would inhibit virus spread in a crop. Africa, as well as a major commercial crop in these regions Morales, Across this area, over million people rely on common bean as a staple crop, and around 3 million tons are produced each year, on almost 5 million ha.

Broughton et al. Beans are a growing part of the export market Beebe et al. For example, snap or French beans are a major export from a number of African countries. Smallholder farmers, who usually intersperse bean with other key crops, produce a considerable proportion of this yield. As an intercrop bean sup- ports cultivation of maize, cassava, and other starch crops by: soil enrichment through nitrogen fixation Broughton et al.

Bean can be highly productive and in some areas within Eastern, Southern, and Central Africa as many as 3 bean crops per year are possible. Per capita consumption of common bean in Africa is the highest globally and bean is estimated to be second and third most important source of die- tary protein and calories, respectively, in Eastern and Southern Africa Broughton et al.

Common bean is consumed across all of its growing stages; in the form of leaves, green pods, as well as fresh and dry grain. Importantly, common beans can be stored dry for long periods, making this crop of critical value for food security in the region CIAT, Bean is a crop of particular economic value to women. In sub-Saharan Africa, bean is often grown and traded by women and it has been noted that in Africa increased wealth creation by female members of the community has a particularly strong positive impact on food security, nutrition, child health, and school attendance rates Kevane, Beans also enrich the diet with several vitamins but perhaps more importantly they provide mineral nutri- ents, most notably iron and zinc, as well as calcium, copper, magnesium, manganese, and phosphorus Broughton et al.

The contribution of iron to the diet is particularly vital in developing countries in which nutri- tional anemia due to iron deficiency is widespread and, among other health impacts, can increase maternal mortality Anon, ; Broughton et al. Fortunately, in parts of Kenya and Uganda, bean consumption is high enough to exceed the minimum dietary iron require- ment, and for many other countries in the region it provides well over half of the requirement Broughton et al. However, bean production in Eastern, Southern, and Central Africa is not currently meeting demand and regionally yields are very low.

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  4. The situation is thought likely to be exacerbated by climate change that could increase challenges to crops from abiotic stresses such as drought or increased biotic attack due to alterations in the range or populations of aphid vectors Canto et al. Bean breeders work- ing within African National Agricultural Research Systems NARS have a wealth of expertise and knowledge about farmer preferences and the con- straints faces by smallholders. A range of resources is available to empower African plant breeders to further their efforts to develop virus-resistant, farmer-preferred varieties.

    In addition to the materials already developed and in use by national breeding programs, CIAT provides breeding materials and other support for incorporation of resistance into varieties by African NARS breeders. For a detailed description of how African NARS breeding programs and their international partners apply these types of approaches, see Kelemu et al.

    National bean breeders of 29 African countries are further supported across the value chain by the Pan African Bean Research Alliance www. Establishment of clean seed supply chains is also a critical focus for addressing the challenge of these seed-transmitted viruses. Contaminated bean seed can provide foci for aphid-mediated transmission. However, lack of reliable tissue culture and regeneration protocols stands in the way of both tissue culture-based production of clean planting materials and inhibit the development of virus- or vector-resistant transgenic bean varieties see Section 7.

    Detailed information about the geographic distribution and genetic diversity of the viruses and their vectors in Africa, however, is lac- king. But in the future this will be required to inform breeding, clean seed production strategies, and other interventions to fight these pathogens. Efforts are underway to characterize the viruses present in bean on small- holder farms in East Africa, which can be extended across the region. To underpin this, the development of appropriate diagnostic tests for use by African breeding programs, phytosanitary organizations, and NARS and African universities is underway.

    New, facile methods of diagnosis under development at the BecA-ILRI Hub include immunodiagnostics, loop- mediated isothermal amplification LAMP , or other assays amenable to use with minimal laboratory equipment or in the field. As we have seen, many potential technical solutions exist or are in development.

    However, a key aspect of deployment of these in Africa must be the engagement and involvement of African scientists as well as the smallholder farmers themselves in developing the most appropri- ate suite of crop protection strategies. We thank Christine Alexander for help with tracking down difficult-to-find references from the older literature. Work on bean- infecting viruses and potyviruses in the labs of J.

    H and J. Mitter is supported by a scholarship from the University of Queensland. Overview and analysis of the poly- protein cleavage sites in the family Potyviridae. Molecular Plant Pathology, 6, — Agbeci, M. Contribution of host intracellular transport machineries to intercellular movement of Turnip mosaic virus. PLoS Pathogens, 9 10 , e Ali, M. Genetics of resistance to the common bean mosaic virus bean virus 1 in the bean Phaseolus vulgaris L.

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    Netherlands Journal of Plant Pathology, 84, 13— Author's personal copy 38 Elizabeth A. Ekpo, E. Distribution pattern of bean common mosaic virus in developing bean seed. Phytopathology, 64, — El-Sawy, M. Serological and molecular characterisations of the Egyptian isolate of Bean common mosaic virus. Archives of Phytopathology and Plant Protection, 47, 1— Fang, G. The complete nucleotide sequence and genome organization of Bean common mosaic virus NL3 strain.

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    Silvestri, S.. Allopurinol, an inhibitor of purine catabolism, enhances susceptibility of tobacco to tobacco mosaic virus. Virus Research Handford, M. Huang, W. Mayers, C. Gilliland, A. Soards, A. Wong, C. Morris, K. Mackerness, S. Taylor, D. O, ap Rees, T. Naylor, M. Surplus, S. M, Naylor, M. Wang, J. Malamy, J. Cutt, J. Xanthi-nc induced by TMV. Berry, J. Antoniw, J. White, R. Plant defense signals: Players and pawns in plant-virus-vector interactions.

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    Viral manipulation of plant stress responses and host interactions with insects. Palukaitis, P. Manipulation of induced resistance to viruses. Current Opinion in Virology Groen, S. Engineering resistance to virus transmission. Current Opinion in Virology — O, Mukeshimana, G. Bean common mosaic virus and Bean common mosaic necrosis virus : Relationships, biology and prospects for control.

    Advances in Virus Research The CMV-Arabidopsis interaction: interplay of viral virulence strategies and plant responses. Sessa, Guido. Signaling in induced resistance. Article addendum. Extracellular ATP. A modulator of cell death and pathogen defense in plants. Journal of Plant Pathology Jane Parker.