1. Please check and comment entries here.
Table of Contents

    Topic review

    Epidemics: Indigenous and Introduced Crops

    Subjects: Plant Sciences
    View times: 23
    Submitted by: Roger jones

    Definition

    Virus disease pandemics and epidemics that occur in the world’s staple food crops pose a major threat to global food security, especially in developing countries with tropical or subtropical climates. Moreover, this threat is escalating rapidly due to increasing difficulties in controlling virus diseases as climate change accelerates and the need to feed the burgeoning global population escalates. One of the main causes of these pandemics and epidemics is the introduction to a new continent of food crops domesticated elsewhere, and their subsequent invasion by damaging virus diseases they never encountered before.

    1. Introduction

    Virus disease epidemics and pandemics threaten all types of cultivated plants including those grown to feed the world’s human population and its domestic animals, and others grown for ornamental, fiber or medicinal uses [1][2][3][4][5][6][7][34][35][36]. Virus epidemics also threaten wild plant communities growing in natural ecosystems [8][9][10][11][12][13]. With crop plants, they diminish the growth and vigor of infected plants, decrease gross yields and disfigure plant produce. The losses they cause vary from total crop failure to smaller scale, occur worldwide and have an estimated economic global impact of >US$30 billion annually [14][15][16][17][18]. They occur in all types of crop plants. These include staple food crops of crucial significance for achieving food security in subtropical and tropical regions [19][20][21][22][23][24][25]. With mixed species-managed pastures and wild plant communities in natural ecosystems, their detrimental effects on the growth and vigor of infected plants alter plant species composition. In managed pastures, they diminish the proportion of pasture plants versus weeds causing pasture deterioration and an inadequate feed base for livestock [26][27][28][29][30][31][32][33]. In wild plant communities, they alter the species balance and decrease species diversity, which damages ecosystems and can cause genetic erosion potentially leading to species extinction [34][35][36][37].

    Development of damaging virus epidemics is favored by the introduction of new crops to parts of the world where they have never been grown before and the adoption of intensive cropping systems both of which lead to new encounters with virulent viruses infecting crops or indigenous vegetation. They are also favored by introduction of vulnerable new cultivars bred for increased yields [38][39][40]. In mixed species-managed pastures, damaging virus epidemics are favored by factors such as relative grazing pressure and trampling by domestic animals resulting in increased insect vector numbers and virus spread by vectors or contact transmission [31][32][33]. In wild plant communities, they are aggravated by factors such as fragmentation into small patches of vegetation enclosed by crops or urban areas, livestock grazing and human disturbance, e.g., woodcutting and flower collection [41].

    Several of the world’s plant virus disease pandemics and major epidemics have resulted from infection with emerging viruses that arose from new encounter situations in which indigenous viruses spread by spillover ( = host species jumps) from infected indigenous plants to infect introduced cultivated plants [42]. However, epidemics can also take place when introduced viruses spread to indigenous plants from infected introduced cultivated plants. Thus, on the one hand, when introduced cultivated plants domesticated elsewhere grow next to indigenous wild plants or locally domesticated crop plants they never encountered previously, indigenous viruses associated with these indigenous hosts can spillover to the introduced crop plants causing virus disease epidemics in them. On the other hand, introduced viruses can also spread to indigenous crop or wild plants from infected introduced cultivated plants or associated weeds, causing virus epidemics. Both types of invasions require virus spread to occur at the interface between indigenous and introduced plants [43][44].

    Pandemics or epidemics occurring in diverse crops and all continents, apart from Antarctica, were documented in a series of reviews written by the late Professor Michael Thresh [45]. These reviews covered the period from the inception of plant virology in the early 1900s up to 2006 [46][47][48][49][50]. In 1980, Thresh [1] provided a review of the origins and epidemiology of a wide range of important plant virus diseases. More up-to-date accounts of damaging pandemics or major epidemics involving several mostly single virus–host–vector pathosystems were described in several recent reviews [51][52][53][54][55][56][57][58]. In addition, a recent review focused on the global dimensions of plant virus disease.

    This review describes virus disease pandemics and major epidemics that arose from spillover scenarios involving new encounters between indigenous viruses and introduced crops, rather than virus spread from introduced crops to indigenous crops or natural vegetation. It does this by providing historical and up-to-date information on five examples of virus diseases that threaten staple food crops critically important for food security in developing countries, placing special emphasis on the situation in sub-Saharan Africa (SSA). The sixth virus disease example threatens livelihoods in SSA because it devastates production of a valuable food export crop. In addition, brief coverage is provided of several other examples of major virus disease epidemics that arose from new encounters between indigenous viruses and introduced crops important for food security in different parts of the world.

    2. General Concepts

    2.1. Definitions

    In his 1970 review of ‘catastrophic plant diseases’, Klinkowski [59] emphasized that many plant disease agents, including viruses, cause epidemics and pandemics, especially when they spread from their centers of origin into continents where they were formerly absent. He defined an epidemic as being “where a disease is spread over an area in which its causal agent has been present for a long time”; a progressive epidemic as “where it expands from this area into others”; and a pandemic as “where epidemics cause mass infections spread over several continents”. He gave five plant virus disease examples: sugarcane mosaic disease spreading worldwide fitted his ‘pandemic’ definition; plum pox, sugar beet yellows and tobacco veinal necrosis diseases spreading mostly in Europe matched his progressive epidemic definition; and cocoa swollen shoot disease (CSSD) spreading in Ghana, West Africa matched his epidemic definition. Subsequently, in plant virology, the term progressive epidemic has fallen into disuse and a plant virus disease pandemic has come to include “an epidemic occurring over a very wide area, crossing international boundaries and causing severe crop losses”. In practice, however, the term epidemic is now widely used to cover all three of these types of epidemic situations, while the term pandemic has become restricted mainly to damaging virus diseases that spread widely between different countries in SSA, e.g., CSSD  and cassava mosaic disease (CMD) and cassava brown streak disease (CBSD). In this review, the ‘pandemic’ definition now mainly used in Africa is also applied to other continents, otherwise the term ‘epidemic’ is used.

    An emerging virus is usually considered to be “one that causes damaging epidemics but has only evolved or been recognized recently, changed its pathogenesis, increased its host range or increased its geographical distribution”. Further, a re-emerging virus is usually considered to be “one that once caused serious disease problems, but then declined in importance before suddenly increasing in incidence and geographical distribution causing considerable crop damage”. Therefore, the term virus emergence refers to “the first appearance of a virus and its associated initial increase in incidence/geographic range”, and the term virus re-emergence refers to “the reappearance of virus and its associated increase in incidence/geographic range”. When the term vulnerable is applied to a crop cultivar, this means that “the cultivar is both susceptible to virus infection (i.e., it becomes infected readily), and sensitive to infection once systemic infection has occurred (i.e., it develops severe symptoms)” [60]. Thus, susceptible is the opposite of resistance and sensitive is the opposite of tolerance [60]. The term virus spillover refers to “spread of a virus from naturally-infected host to a new host it has not encountered previously”, and the term spillback refers to “spread of a virus from the new host back to the natural host” .

    2.2. Crop Domestication Centers and Introductions

    Selection of local land races of crop plants from wild ancestors commenced more than 10,000 years ago in the worlds’ plant domestication centers [61][62]. Viruses from these wild ancestors were present among the land races derived from them and these indigenous viruses adapted to their new situation multiplying in cultivated plants growing mostly in mixed species cultivation. Later, through international trade, crop plants were moved progressively away from their domestication centers to distant continents where they were often grown as monocultures. For example, the Columbian Exchange was responsible for the introduction of crops critical for food security to other continents following the Spanish 1492 arrival in the Americas, such as maize (Zea mays), cassava (Manihot esculenta), potato (Solanum tuberosum) and tomato (Solanum lycopersicum) [63]. In consequence, new encounters between introduced cultivated plants, and infected wild or crop plants occurred resulting in spillover of indigenous viruses into introduced crops. Sometimes epidemics arose soon afterwards and sometimes only after a considerable delay triggered by other factors, and some later became pandemics.

    2.3. Factors Favoring Spillover

    Successful spillover starts with spread of already existing genetic virus variants from a virus infection source plant to the new host plant, and the outcome for each individual variant depends on its relative abilities (i.e., fitness) to survive once it infects each host, adapt to new hosts or vectors and achieve efficient epidemic spread [64]. A range of factors favor successful virus spillover, emergence or re-emergence. These include: presence of efficient indigenous or introduced virus vectors, including “supervectors”; introduction of vulnerable crop cultivars; adoption of cultural practices involving agricultural intensification, extensification and diversification; intensive wildflower production and conservation projects; the relative ability of a virus to generate virulent new variants through mutation, reassortment and recombination; and climate change arising from global warming [65][66][67][68][69][70][71][72][73][74][75][76][77][78][79].

    This entry is adapted from 10.3390/v12121388

    References

    1. Thresh, J.M. The origins and epidemiology of some important plant virus diseases. Appl. Biol. 1980, 5, 1–65.
    2. Thresh, J.M. Crop viruses and virus diseases: A global perspective. In Virus Diseases and Crop Biosecurity; Cooper, J.I., Kuehne, T., Polischuk, V.P., Eds.; Springer: Dordrecht, The Netherlands, 2006; pp. 9–32.
    3. Anderson, P.K.; Cunningham, A.A.; Patel, N.G.; Morales, F.J.; Epstein, P.R.; Daszak, P. Emerging infectious diseases of plants: Pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 2004, 19, 535–544. [CrossRef]
    4. Jones, R.A.C. Plant virus emergence and evolution: Origins, new encounter scenarios, factors driving emergence, effects of changing world conditions, and prospects for control. Virus Res. 2009, 141, 113–130. [CrossRef] [PubMed]
    5. Jones, R.A.C. Plant virus ecology and epidemiology: Historical perspectives, recent progress and future prospects. Ann. Appl. Biol. 2014, 164, 320–34
    6. Hull, R. Mathews’ Plant Virology, 5th ed.; Academic Press: London, UK, 2014.
    7. Jones, R.A.C.; Naidu, R.A. Global dimensions of plant virus diseases: Current status and future perspectives. Annu. Rev. Virol. 2019, 6, 387–409. [CrossRef] [PubMed]
    8. Bos, L.Wild plants in the ecology of virus diseases. In Plant Diseases and Vectors: Ecology and Epidemiology; Maramarosch, K., Harris, K.F., Eds.; Academic Press: New York, NY, USA, 1981; pp. 1–8.
    9. Thresh, J.M. (Ed.) Pests, Pathogens and Vegetation; Pitman: London, UK, 1981.
    10. Cooper, J.I.; Jones, R.A.C. Wild plants and viruses: Under-investigated ecosystems. Adv. Virus Res. 2006, 67, 1–47.
    11. Alexander, H.M.; Mauck, K.E.; Whitfield, A.M.; Garrett, K.A.; Malmstrom, C.M. Plant-virus interactions and the agro-ecological interface. Eur. J. Plant Pathol. 2014, 138, 529–547. [CrossRef]
    12. Jones, R.A.C.; Coutts, B.A. Spread of introduced viruses to new plants in natural ecosystems and the threat this poses to plant biodiversity. Mol. Plant Pathol. 2015, 16, 541–545. [CrossRef] [PubMed]
    13. Malmstrom, C.M.; Alexander, H.M. Effects of crop viruses on wild plants. Curr. Opin. Virol. 2016, 19, 30–36. [CrossRef]
    14. Bos, L. Crop losses caused by viruses. Crop Prot. 1982, 1, 263–282. [CrossRef]
    15. Jones, R.A.C. Using epidemiological information to develop effective integrated virus disease management strategies. Virus Res. 2004, 100, 5–30. [CrossRef] [PubMed]
    16. Jones, R.A.C. Control of plant virus diseases. Adv. Virus Res. 2006, 67, 205–244. [PubMed]
    17. Sastry, S.K.; Zitter, T.A. Management of virus and viroid diseases of crops in the tropics. In Plant Virus and Viroid Diseases in the Tropics, Volume 2, Epidemiology and Management; Sastry, S.K., Zitter, T.A., Eds.; Springer:Dordrecht, The Netherlands, 2014; pp. 149–480.
    18. Jeger, M.J.; Thresh, J.M. Modelling reinfection of replanted cocoa by swollen shoot virus in pandemically diseased areas. J. Appl. Ecol. 1993, 30, 187–196. [CrossRef]
    19. Thresh, J.M. Control of tropical plant virus diseases. Adv. Virus Res. 2006, 67, 245–295.
    20. Thresh, J.M. Plant virus epidemiology: The concept of host genetic vulnerability. Adv. Virus Res. 2006, 67, 89–125.
    21. Brunt, A.; Crabtree, K.; Gibbs, A.J. Viruses of Tropical Plants: Descriptions and Lists from the VIDE Database: CAB International: Wallingford, UK, 1990.
    22. Bos, L. New plant virus problems in developing countries: A corollary of agricultural modernization. Adv. Virus Res. 1992, 41, 349–407.
    23. Otim-Nape, G.W.; Thresh, J.M. The current pandemic of cassava mosaic virus disease in Uganda. In The Epidemiology of Plant Diseases; Jones, G., Ed.; Kluwer: Dordrecht, The Netherlands, 1998; pp. 423–443
    24. Mahuku, G.; Lockhart, B.E.; Wanjala, B.; Jones, M.W.; Kimunye, J.N.; Stewart, L.R.; Cassone, B.J.; Sevgan, S.; Nyasani, J.O.; Kusia, E.; et al. Maize lethal necrosis (MLN), an emerging threat to maize-based food security in sub-Saharan Africa. Phytopathology 2015, 105, 956–965. [CrossRef]
    25. Oliver, J.E.; Whitfield, A.E. The genus Tospovirus: Emerging bunyaviruses that threaten food security.Annu. Rev. Virol. 2016, 3, 101–124. [CrossRef]
    26. Catherall, P.L. Effects of barley yellow dwarf and ryegrass mosaic viruses alone and in combination on the productivity of perennial and Italian ryegrass. Plant Pathol. 1987, 36, 73–78. [CrossRef]
    27. McLaughlin, M.R.; Pederson, G.A.; Evans, R.R.; Ivy, R.L. Virus diseases and stand decline in a white clover pasture. Plant Dis. 1992, 76, 158–162. [CrossRef]
    28. Jones, R.A.C.; Nicholas, D.A. Impact of an insidious virus disease in the legume component on the species balance within self-regenerating annual pasture. J. Agric. Sci. Camb. 1998, 131, 155–170. [CrossRef]
    29. Eagling, D.R.; Villalta, O.; Sward, R.J. Host range, symptoms and e_ects on pasture production of a Victorian isolate of ryegrass mosaic potyvirus. Aust. J. Agric. Res. 1992, 43, 1243–1251. [CrossRef]
    30. Coutts, B.A.; Jones, R.A.C. Temporal dynamics of spread of four viruses within mixed species perennial pastures. Ann. Appl. Biol. 2002, 140, 37–52. [CrossRef]
    31. Jones, R.A.C. Virus diseases of annual pasture legumes: Incidences, losses, epidemiology and management. Crop Pasture Sci. 2012, 63, 399–418. [CrossRef]
    32. Jones, R.A.C. Virus diseases of perennial pasture legumes: Incidences, losses, epidemiology and management. Crop Pasture Sci. 2013, 64, 199–215. [CrossRef]
    33. Jones, R.A.C.Virus diseases of pasture grasses in Australia: Incidences, losses, epidemiology and management. Crop Pasture Sci. 2013, 64, 216–233. [CrossRef]
    34. Malmstrom, C.M.; Hughes, C.C.; Newton, L.A.; Stoner, C.L. Virus infection in remnant native bunchgrasses from invaded California grasslands. New Phytol. 2005, 168, 217–230. [CrossRef]
    35. Malmstrom, C.M.; McCullough, A.J.; Johnson, H.A.; Newton, L.A.; Borer, E.T. Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses. Oecologia 2005, 145, 153–164. [CrossRef]
    36. Malmstrom, C.M.; Bigelow, P.; Tr˛ebicki, P.; Busch, A.K.; Friel, C.; Cole, E.; Abdel-Azim, H.; Phillippo, C.;lexander, H.M. Crop-associated virus reduces the rooting depth of non-crop perennial native grass more than non-crop-associated virus with known viral suppressor of RNA silencing (VSR). Virus Res. 2017, 241, 172–184. [CrossRef]
    37. Vincent, S.J.; Coutts, B.A.; Jones, R.A.C. Effects of introduced and indigenous viruses on native plants: Exploring their disease causing potential at the agro-ecological interface. PLoS ONE 2014, 9, e91224.
    38. Thresh, J.M. Control of plant virus diseases in sub-Saharan Africa: The possibility and feasibility of an integrated approach. Afr. Crop Sc. J. 2003, 11, 199–223. [CrossRef]
    39. Loebenstein, G.; Thottappilly, G. (Eds.) Virus and Virus-like Diseases of Major Crops in Developing Countries; Springer: Dordrecht, The Netherlands, 2013.
    40. Thresh, J.M. Cropping practices and virus spread. Annu. Rev. Phytopathol. 1982, 20, 193–218. [CrossRef]
    41. Jones, R.A.C.; Barbetti, M.J. Influence of climate change on plant disease infections and epidemics caused by viruses and bacteria. Plant Sci. Rev. 2012, 22, 1–31. [CrossRef]
    42. Roossinck, M.J.; García-Arenal, F. Ecosystem simplification, biodiversity loss and plant virus emergence. Curr. Opin. Virol. 2015, 10, 56–62. [CrossRef]
    43. Webster, C.G.; Coutts, B.A.; Jones, R.A.C.; Jones, M.G.K.;Wylie, S.J. Virus impact at the interface of an ancient ecosystem and a recent agroecosystem: Studies on three legume-infecting potyviruses in the South West Australian Floristic Region. Plant Pathol. 2007, 56, 729–742. [CrossRef]
    44. Faillace, C.A.; Lorusso, N.S.; Du_y, S. Overlooking the smallest matter: Viruses impact biological invasions. Ecol. Lett. 2017, 20, 524–538. [CrossRef]
    45. Irwin, M.E.; Fereres, A. John Michael Thresh, founding father of plant virus epidemiology: A tribute. Virus Res. 2017, 241, 3–9. [CrossRef]
    46. Thresh, J.M. An ecological approach to the epidemiology of plant virus diseases. In Comparative Epidemiology: A Tool for Better Disease Management; Palti, J., Kranz, J., Eds.; Centre for Agricultural Publishing and Documentation: Wageningen, The Netherlands, 1980; pp. 57–70.
    47. Thresh, J.M. Plant virus epidemiology and control: Current trends and future prospects. In Plant Virus Epidemiology—The Spread and Control of Insect-Borne Pathogens; Plumb, R.T., Thresh, J.M., Eds.; Blackwell: Oxford, UK, 1983; pp. 349–360.
    48. Thresh, J.M. Insect-borne viruses of rice and the Green Revolution. Int. J. Pest Manag. 1989, 35, 264–272.[CrossRef]
    49. Thresh, J.M. Plant virus epidemiology: The battle of the genes. In Recognition and Response in Plant-Virus Interactions; [NATO ASI Series H: Cell Biology]; Springer: Heidelberg, Germany, 1990; Volume 41, pp. 93–121.T
    50. Thresh, J.M. The ecology of tropical plant viruses. Plant Pathol. 1991, 40, 324–339. [CrossRef]
    51. Dombrovsky, A.; Tran-Nguyen, L.T.T.; Jones, R.A.C. Cucumber Green Mottle Mosaic Virus: Rapidly increasing global distribution, etiology, epidemiology, and management. Annu. Rev. Phytopathol. 2017, 55, 231–256.[CrossRef]
    52. Moriones, E.; Praveen, S.; Chakraborty, S. Tomato leaf curl New Delhi virus: An emerging virus complex threatening vegetable and fibre crops. Viruses 2017, 9, 264. [CrossRef] [PubMed]
    53. Rey, C.; Vanderschuren, H. Cassava mosaic and brown streak diseases: Current perspectives and beyond. Annu. Rev. Virol. 2017, 4, 429–452. [CrossRef] [PubMed]
    54. Fargette, D.; Konate, G.; Fauquet, C.; Muller, E.; Peterscmitt, M.; Thresh, J.M. Molecular ecology and
    55. emergence of tropical plant viruses. Ann. Rev. Phytopathol. 2006, 44, 235–260. [CrossRef] [PubMed]
    56. Redinbaugh, M.G.; Stewart, L.R. Maize lethal necrosis: An emerging, synergistic viral disease.
    57. Annu. Rev. Virol. 2018, 5, 301–322. [CrossRef]
    58. Tomlinson, K.R.; Bailey, A.M.; Alicai, T.; Seal, S.; Foster, G.D. Cassava brown streak disease: Historical
    59. timeline, current knowledge and future prospects. Mol. Plant Pathol. 2018, 19, 1282–1294. [CrossRef]
    60. Fiallo-Olivé, E.; Navas-Castillo, J. Tomato chlorosis virus, an emergent plant virus still expanding its
    61. geographical and host ranges. Mol. Plant Pathol. 2019, 20, 1307–1320. [CrossRef]
    62. Klinkowski, M. Catastrophic plant diseases. Ann. Rev. Phytopathol. 1970, 8, 37–60. [CrossRef]
    63. Cooper, J.I.; Jones, A.T. Responses of plants to viruses: Proposals for the use of terms. Phytopathology 1983,73, 127–128. [CrossRef]
    64. Harlan, J.R. Agricultural origins: Centres and non-centres. Science 1971, 174, 468–474. [CrossRef]
    65. Harlan, J.R. Ecological settings for the emergence of agriculture. In Pests, Pathogens and Vegetation; Thresh, J.M., Ed.; Pitman Press: London, UK, 1981; pp. 3–22.
    66. Nunn, N.; Qian, N. The Columbian Exchange: A history of disease, food, and ideas. J. Econ. Perspect. 2010, 24, 163–188. [CrossRef]
    67. Elena, S.F.; Fraile, A.; Garcia-Arenal, F. Evolution and emergence of plant viruses. Adv. Virus Res. 2014, 88, 161–191. [PubMed]
    68. Rojas, M.R.; Gilbertson, R.L. Emerging plant viruses: A diversity of mechanisms and opportunities. In
    69. Plant Virus Evolution; Roossinck, M.A., Ed.; Springer: Berlin/Heidelberg, Germany, 2008; pp. 27–51.
    70. Pagán, I.; González-Jara, P.; Moreno-Letelier, A.; Rodelo-Urrego, M.; Fraile, A.; Piñero, D.; García-Arenal, F. Effect of biodiversity changes in disease risk: Exploring disease emergence in a plant-virus system. PLoS Pathog. 2012, 8, e1002796. [CrossRef] [PubMed]
    71. Fereres, A. Insect vectors as drivers of plant virus emergence. Curr. Opin. Virol. 2015, 10, 42–46. [CrossRef] [PubMed]
    72. Gilbertson, R.L.; Batuman, O.;Webster, C.G.; Adkins, S. Role of the insect supervectors Bemisia tabaci and Frankliniella occidentalis in the emergence and global spread of plant viruses. Annu. Rev. Virol. 2015, 2, 67–93. [CrossRef]
    73. Jones, R.A.C. Future scenarios for plant virus pathogens as climate change progresses. Adv. Virus Res. 2016,95, 87–147.
    74. Jones, R.A.C. Plant and insect viruses in managed and natural environments: Novel and neglected
    75. transmission pathways. Adv. Virus Res. 2018, 101, 149–187.
    76. García-Arenal, F.; Zerbini, F.M. Life on the edge: Geminiviruses at the interface between crops and wild plant hosts. Annu. Rev. Virol. 2019, 6, 411–433. [CrossRef]
    77. McLeish, M.J.; Fraile, A.; García-Arenal, F. Evolution of plant–virus interactions: Host range and virus
    78. emergence. Curr. Opin. Virol. 2019, 34, 50–55. [CrossRef]
    79. Lefeuvre, P.; Martin, D.P.; Elena, S.F.; Shepherd, D.N.; Roumagnac, P.; Varsani, A. Evolution and ecology of plant viruses. Nat. Rev. Microbiol. 2019, 17, 632–644. [CrossRef]
    More