Particle of Ornithogalum mosaic virus (OrMV)
Ed Rybicki and Gerhard Pietersen
October 2000
This material is excerpted and modified from:
"Rybicki EP, Pietersen G (1999) Plant virus disease
problems in the developing world. Advances in Virus Research 53: 128-175"
There are three major groups of viruses that seem to be most important among new disease-causing agents worldwide, and that could reasonably be termed "emerging" in terms of apparently being new viruses causing new and serious diseases. The most important of these are in the taxonomic families Potyviridae and Geminiviridae, the Tospovirus genus of the Bunyaviridae, and perhaps also pararetroviruses like Banana streak virus (BSV).
The Potyviridae are the largest single taxonomic group of plant viruses, and the subject of more scientific papers per year than any other plant virus taxonomic group except perhaps the geminiviruses. It seems that potyviruses, and specifically aphid-transmitted viruses of the genus Potyvirus, are one of the most successful groups of plant pathogens in the world. The genus has been claimed to be almost as ancient as flowering plants, and has a worldwide distribution throughout higher plants. New potyviruses seem to appear with new crop introductions just about anywhere these occur. In South Africa, for example, Passiflora edulis (passionfruit) cultivation in the 1980s was severely limited by diseases, many of which appeared linked to a mixture of potyvirus-like agents. One of these viruses was characterized here in detail and found to be not the passionfruit woodiness virus (PWV) characterized in Australia and the Far East, but a distinct species now known to be a strain of cowpea aphid-borne mosaic virus (CABMV). It is very interesting that a similar disease in Brazil seems to be caused by a closely-related strain of the same virus, whereas woodiness disease in Australasia and Asia is caused by distinct species of viruses.
Another intriguing aspect of emerging potyviral plant diseases is the appearance of hitherto latent virus infections. A well-documented case investigated here was the appearance in cultivated specimens of the horticulturally important flowering bulbs Ornithogalum and Lachenalia species of at least two distinct potyviruses. One of these, Ornithogalum mosaic virus (OrMV), first described in South African-derived bulbs in Holland, was found in plant specimens collected in localities where the plants were endemic. However, it caused apparent or overt infections only when plants were kept in cultivation.
Particle of Ornithogalum mosaic virus (OrMV)
Viruses in the family Geminiviridae, and specifically the whitefly-transmitted begomoviruses, are presently associated with severe diseases in tomatoes the world over, with cotton disease in India and elsewhere, and with disease problems and food shortages due to disease in cassava in central Africa. Infections with Bean golden mosaic virus (BGMV) are apparently the single largest limiting factor to bean production in Central America.
Polston and Anderson (1997) covered the Caribbean basin and the Central American region in an excellent review of the emergence of whitefly-transmitted geminiviruses (WTGs) in tomatoes. They estimated that 20 - 100% of crop loss throughout these areas has been caused by epidemics of WTGs, ranging from Tomato golden mosaic (TGMV) to Tomato yellow leaf curl (TYLCV) to Potato yellow mosaic (PYMV). They listed 17 distinct viruses known to affect tomatoes in this region, and this is probably a conservative estimate, as more are constantly being found.
Much of the apparently emerging nature of the virus diseases is due to the worldwide spread of a new "silverleaf" or B biotype of the vector Bemisia tabaci, which is now being touted as the new species Bemisia argentifolii. The new vector has a much wider range of preferences for feeding than older vector types, which has apparently resulted in the spread of viruses that normally infect only weed or endemic plant species into adjacent, previously untargeted crop species. Roye et al. (1997) surveyed geminiviruses in weeds (notably Sida and Wissadula species) in Jamaica and showed a population of viruses distinct from crop-infecting geminiviruses - and one perhaps poised to enter crops once a suitable vector biotype appears. Although the problem also exists in the developed world , and most notably in the southern United States and Europe, it can be dealt with, to at least some extent, by changing cultivation practices. The same option does not exist in the developing world, however, due to the expensive nature of the measures (screen houses, heavy spraying regimes). Thus, the inexorable spread of the vector into these areas will almost certainly mean heavy crop losses.
This may have already happened in cassava in Uganda and western Kenya; however, the disease problem there is also associated with a natural recombinant virus (between African cassava mosaic virus, ACMV, and East African cassava mosaic virus, EACMV) with increased virulence. The scale of the problem was aptly illustrated by an anonymous agricultural researcher from Uganda, who said (to E.P. Rybicki, in 1997) that there was no cassava disease problem in eastern Uganda, as there was no more cassava to be infected!
Severe leaf distortion and mosaic and leaf loss in cassava in western Kenya caused by African cassava mosaic virus / East African cassava mosaic virus recombinant. Inset: healthy leaf. Photos by EP Rybicki, 1997
Begomovirus diseases also seem to exemplify a phenomenon first noted with potyviruses; unrelated or distinct virus species in the genus cause very similar disease syndromes in the same crop plants, usually in widely separated geographical areas but sometimes in the same small area. Thus, TYLCV-Israel, -Sardinia, and -Thailand are distinct species of virus despite causing the same disease; however, so are the several viruses causing cotton leaf curl disease in India and Pakistan, and the several distinct viruses causing tomato leaf curl in India. This is undoubtedly related to their worldwide distribution and also to their apparent antiquity. Geminivirus variation appears linked to geographic separation and host plant genetic divergence, as well as to continental drift (Rybicki, 1994). All these factors indicate that the youngest age for the family Geminiviridae is hundreds of millions of years and that of begomoviruses is at least tens of millions of years. This diversity and ubiquity guarantee that a wide variety of virus genotypes exists, probably as well-adapted and essentially symptomless infections in endemic species or weeds, and that any change in transmission characteristics of the vector will result in appearance of the virus in crop plants almost instantly.
Whereas begomoviruses have been making their presence felt as they spread out of endemic hosts into cultivated species, viruses in the genus Mastrevirus continue to emerge into crop species in Africa. Maize streak disease (MSD) was first described in 1901, so can hardly be considered as emerging. However, more recent findings indicate that a hitherto unsuspected and distinct group of Maize streak virus (MSV) strains cause disease in wheat and some grasses, rather than the disease being caused by the same closely-related group of virus isolates and strains as are found in maize (Rybicki et al., 1998; see also here). Sugarcane streak virus(es) (SSVs) also still seem to be present in Africa. Whereas the better characterized variants SSV-Natal and SSV-Mauritius have not been a problem in southern Africa for over 30 years, and especially not in commercially-grown sugarcane varieties, distinct mastrevirus species have recently been characterized from mildly diseased "traditional" material from Egypt (Bigarré et al., 1999).
A ray of hope in the struggle to combat TYLCV-like diseases is the fact that genetic engineering approaches using pathogen-derived resistance appear to be quite promising. Tomato plants transgenic for the TYLCV coat protein appear to be resistant to the virus (Kunik et al., 1994). Additionally, transgenic Nicotiana benthamiana plants expressing antisense RNA to the Rep gene were resistant to TYLCV infection (Bendahmane and Gronenborn, 1997). These developments, coupled with traditional and marker-assisted breeding techniques, may allow rapid dissemination of improved material to farmers.
The genus Tospovirus (family Bunyaviridae) is an extremely important group of plant viruses capable of infecting a large range of important crops. The type member, Tomato spotted wilt virus (TSWV), has one of the broadest host ranges among plant viruses. Tospoviruses are transmitted exclusively by thrips in a circulative propagative manner, meaning that the virus multiplies in the vector. TSWV was thought to be the only member of this genus until recently, and has had a serious impact on many crop species worldwide. It causes severe outbreaks in a large variety of crops grown in tropical and subtropical climate zones. Since 1990, other related but distinct viruses in this genus have been identified. The following members or tentative members are described: TSWV, Groundnut ringspot virus (GRSV), Tomato chlorotic spot virus (TCSV), Impatiens necrotic spot virus (INSV), Watermelon silver mottle virus (WSMV), and Groundnut bud necrosis virus (GBNV).
Owing to the worldwide spread of the Western flower thrip (Frankliniella occidentalis Pergande), the most efficient vector of tospoviruses, TSWV and some of the other tospoviruses are increasing being reported as causing problems in developing countries. These "new" tospoviruses often originate in developing countries, and some appear to occur only in these countries. For example, GRSV was first detected on peanuts during a survey of the viruses of this crop in South Africa, and isolate SA-05 now serves as the type isolate of GRSV. Thus far, this virus has been detected only on peanuts in South Africa, where it is relatively common, and on tomatoes in Brazil and Argentina. TCSV was first reported from Brazil, and GBNV was first detected in India.
Research on this important virus group has increased dramatically, and new tospoviruses are constantly being found. It could be that only the lack of resources in developing countries for the diagnosis of hard-to-identify viruses prevents even more reports of new tospoviruses.
Banana streak virus (BSV) is a pararetrovirus - that is, a virus with circular dsDNA in virions which replicates via a longer-than-genome-length ssRNA(+) intermediate, via reverse transcription (see here). BSV may be considered an emerging problem in light of recent findings suggesting, first, that it occurs in an integrated form in Musa (see here); second, that it has been found in this form in all Musa germplasm tested thus far; third, that it is seed transmitted; and fourth, that the integrated virus can be activated to form the episomal form through stress. Stress can possibly include tissue culture propagation. Thus, it may be that initial BSV infections may largely be the result of plant stress, which means that BSV infections could occur anywhere, at any time, in the absence of any vectored introduction. It may be that genetic engineering in the form of a "knock-out" of the integrated viral genome can come to the rescue, at least of major commercial varieties.
