NOTE: this has now been published, and is citable, at:
Archives of Virology
A Top Ten list for economically important plant viruses
The new version can also be downloaded here: https://www.researchgate.net/publication/268879490_A_Top_Ten_list_for_economically_important_plant_viruses
A recent MicrobiologyBytes post reported a slightly older Molecular Plant Pathology paper as giving a “Top Ten” ranking for plant viruses – at least, those of “…perceived importance, scientifically or economically, from the views of the contributors to the journal”. Specifically, the article authors “…survey[ed] all plant virologists with an association with Molecular Plant Pathology and ask[ed] them to nominate which plant viruses they would place in a ‘Top 10’ based on scientific/economic importance”. They got “…more than 250 votes from the international community”, and came up with the following list:
(1) Tobacco mosaic virus (TMV),
(2) Tomato spotted wilt virus (TSWV),
(3) Tomato yellow leaf curl virus (TYLCV),
(4) Cucumber mosaic virus (CMV),
(5) Potato virus Y (PVY),
(6) Cauliflower mosaic virus (CaMV),
(7) African cassava mosaic virus (ACMV),
(8) Plum pox virus (PPV),
(9) Brome mosaic virus (BMV) and
(10) Potato virus X (PVX),
with honourable mentions for viruses just missing out on the Top 10, including Citrus tristeza virus (CTV), Barley yellow dwarf virus (BYDV), Potato leafroll virus (PLRV) and Tomato bushy stunt virus (TBSV).
Yes, well. Um. Now I have an acquaintance with Molecular Plant Pathology – a recent review and an Editorship on the short-lived MPP Online – as well as knowing 6 of the 12 authors personally and being electronically acquainted with another two, and I was never asked…. And Brome mosaic?? Sweet little virus, and I spent some 7 years working on it (a major part of my Hons, MSc and PhD theses, since you ask), but important?? Cauliflower mosaic, too: great virus; tough as an old boot, supplied one of the most used promoters (35S) for plant expression – but economically important??
Now I am in the position of having worked quite a lot with four of the Top Ten plus alternates (namely, TMV, CMV, BMV and BYDV), and maintain an affection borne of long acquaintance – yet I have a problem with this list, and it is rather fundamental. You see, I see only ONE virus in the major list – African cassava mosaic begomovirus (ACMV) – that infects and causes severe losses in one of the four major food crops grown on this planet: all the rest, excepting viruses infecting the also-ran potato, are pathogens of fruits, vegetables or horticulturally-important plants. Or hardly pathogenic at all, as in the case of BMV – and before anyone argues, I probably have the best collection of African (and other) isolates of the virus in the world, and a lot of experience of it in the field.
I wrote this as a response to the MicrobiologyBytes blog post:
Interesting list – but wrong, as many of these things often are. TYLCV more important than the various African cassava geminiviruses?? Nonsense! And where is Maize streak virus – the most important viral pathogen of the most important crop plant in Africa? Where too the rice viruses?? The world’s top food crops are rice, maize, wheat, cassava and bananas – so what about Maize rayado fino virus, Rice dwarf…? Banana bunchy top or banana streak? I can bet the majority of the plant virologists polled (I was not, nor was anyone I know from around these parts) were from the developed world, and the northern hemisphere.
Gary Foster – the last and communicating author – replied:
Not a case of ‘wrong’, more a case of many forms of ‘right’.
in the review we state….’we are very much aware that importance and priorities can vary locally across continents and disciplines.’ But in the review we took a global snapshot.
The idea was to promote discussion, and I knew you would take up the challenge ;-)
“People could vote on either scientific or economic importance. BMV is in Top 10 because of scientific importance as it states in the article….NOT economic.”
So here we go in taking up the challenge…! First off, I think having a list of viruses where the economic importance ranges from “Major” through “Minor” to “Beneath Notice” is a cop-out, because it elevates scientific curiosities and sentimental favourites to equal or greater perceived importance to plant viruses that can actually lead to people dying. I wrote in 1999, with my friend and colleague Gerhard Pietersen, a paper entitled “Plant virus disease problems in the developing world” (Rybicki EP, Pietersen, G; Adv Virus Res. 1999;53:127-75). We took the view that the most important plant viruses in the world were those affecting the major food crops in the developing world specifically, seeing as these would affect the greatest number of people, and would probably be the least well controlled. Our list, therefore, looks nothing like the one above.
Mrs Pauline Ruiru, on her farm near Githungiri, Kenya, in 1997 – note the devastated maize infected with MSV
In 1999, we wrote the following:
“The Food and Agriculture Organisation (FAO) has defined the major primary food crops (in order of volume grown ) in the developing world to be: (1) rice, (2) wheat, (3) maize, (4) cassava, (5) fresh vegetables, and (6) sweet potatoes. Other crops of major importance are sugarcane, oil palm fruit and soybeans. The most important crops in the developing world as far as local populations are concerned, however, are bulk foods such as rice, maize, cassava, bananas, and sweet potatoes; vegetables such as beans and pumpkins; and fruits such as mangoes and coconuts”.
So: no tobacco, precious few tomatoes or potatoes, definitely no wheat, precious few things that could be affected by PPV…and 8 of the Top Ten gone, at a stroke. I’ll allow the ACMD (African cassava mosaic disease) complex [note: NOT ACMV], and CMV, seeing as it infects damn nearly anything, including maize and most vegetables.
Another problem with the list as given above is that “TYLCV” is in fact better represented by a complex of reasonably distantly related geminiviruses which do similar things to tomatoes, in very different geographic areas: thus, we have the original TYLCV, as well as TYLC Sardinia V, and TYLCCNV and TYLCTHV – all separate species. The supposed “ACMV” is probably neither the best studied nor even the most interesting of the ACMD agents: the East African CMV – ACMV recombinant virus which caused an epiphytotic in Uganda was far more economically important than ACMV, and has been followed in the literature (and in the field) by a host of brethren, all distantly enough related to be separate species (eg: SACMV), but all causing what looks like ACMD.
So what is my Top Ten? I would not go as far – without researching and writing another review – as ranking them; however, from the basis of considering only viruses with sufficient economic impact to kill people if crops are affected, it would be these – ordered by crop importance.
Rice: the rice tungro disease agents RTBV, a dsDNA badnavirus, and rice tungro spherical virus RTSV, an ssRNA waikavirus, in Asia. Rice yellow mottle (RYMV) ssRNA sobemovirus in Africa. Rice hoja blanca virus (RHBV, ssRNA(-) Tenuivirus) in South America.
Wheat: Barley yellow dwarf luteoviruses (BYDV) – again, actually a complex of ssRNA viruses which in fact belong in different species – is almost certainly the worst viral pathogen of wheat worldwide.
A cryoEM image reconstruction of an MSV particle (Kyle Dent, EM Unit, UCT)
Maize: the ssDNA geminiviral pathogen Maize streak mastrevirus (MSV) is the worst viral pathogen of maize in the whole of Africa, where maize is the the most common staple food. A recent review from our group – in Molecular Plant Pathology, I will note – details the very significant economic impact of the virus, as well as the considerable body of molecular virological research on it. We wrote in 2009:
“Maize streak disease (MSD) was first recorded in South Africa by Claude Fuller (1901), the Government Entomologist of Natal. Fuller also quoted personal sources who noticed the disease of ‘mealie variegation’, as it was then described, as early as the 1870s. …Over 100 years later, MSD remains the most significant viral disease of Africa’s most important food crop (Bosque-Pérez, 2000), costing between US$120M and US$480M per year according to one conservative estimate based on average annual yield losses of only 6%–10%”. As losses can be up to 100%, this is almost certainly an underestimate – Ed.
Staying with maize, Maize rayado fino virus (MRFV, ssRNA Marafivirus) is possibly the most important virus in North and especially South America. The ssRNA potyviruses Maize dwarf mosaic and Sugarcane mosaic viruses are probably the most widespread viruses of maize, having essentially a worldwide distribution, and often being associated with severe disease.
Sweet potato: Sweet potato feathery mottle potyvirus (SPFMV) is probably the worst pathogen affecting this increasingly used crop worldwide, but pathology is exacerbated by co-infection with Sweet potato sunken vein closterovirus (SPSVV).
Main picture: cassava plant showing the effects of severe ACMD. Note lack of leaves, and of neighbouring plants. Insets, top: healthy leaves; middle, mild infection; bottom, severe infection. All photographs by EP Rybicki, taken in western Kenya, June, 1997
Cassava: the Africa-limited ACMD complex of ACMV, EACMV, SACMV and others together constitute a major threat to food security in the continent, especially given an increased use of cassava continent-wide. As an object example of why I choose to go with the viruses mentioned, it is worth revisiting something I wrote in 1999:
“It is quite remarkable to pass within a few kilometers from areas with mild ACMD to areas where there are almost no cassava plants left growing. The inevitable lag in replacement of the crop by sweet potato, for example, results in severe hardship for farming families accustomed to using it as a staple in their diet. The wave of ACMD across Uganda may be a good example of the devastating effect of a plant virus on the human population.”
Twelve years on, I see no reason to revise the statement.
Bananas: the worst virus affecting bananas worldwide has to Banana bunchy top nanovirus (BBTV): this ssDNA pathogen has been identified in numerous developing countries in Oceania, Africa, and Asia and has caused devastating epidemics. Also-rans include the dsDNA Banana streak badnavirus (BSV) – also found integrated into the genome of many Musa spp. – and the ssRNA Cucumber mosaic cucumovirus (CMV).
So, the Rybicki Top Ten (in alphabetical order):
- African cassava mosaic disease begomovirus complex
- Banana bunchy top nanovirus (BBTV)
- Banana streak badnavirus (BSV)
- Barley yellow dwarf disease luteovirus complex
- Cucumber mosaic cucumovirus (CMV: OK, reluctantly, because it DOES infect damn nearly anything)
- Maize streak mastrevirus (MSV)
- Maize dwarf mosaic / Sugarcane mosaic potyviruses
- Rice tungro disease complex
- Rice yellow mottle sobemovirus (RYMV)
- Sweet potato feathery mottle potyvirus (SPFMV)
- The legion of tomato begomoviruses worldwide, but especially in Asia
- Tomato spotted wilt tospovirus, because it IS still an emerging virus
- Various South American (mainly Brazilian) vegetable begomoviruses
- Various potyviruses, mainly in vegetables, in Asia
So there it is – viruses causing severe hardship, affecting real people. And my affectionate favourite would also be BMV…B-)