Global Plant Virus Disease Pandemics and Epidemics

Abstract

The world's staple food crops, and other food crops that optimize human nutrition, suffer from global virus disease pandemics and epidemics that greatly diminish their yields and/or produce quality. This situation is becoming increasingly serious because of the human population's growing food requirements and increasing difficulties in managing virus diseases effectively arising from global warming. This review provides historical and recent information about virus disease pandemics and major epidemics that originated within different world regions, spread to other continents, and now have very wide distributions. Because they threaten food security, all are cause for considerable concern for humanity. The pandemic disease examples described are six (maize lethal necrosis, rice tungro, sweet potato virus, banana bunchy top, citrus tristeza, plum pox). The major epidemic disease examples described are seven (wheat yellow dwarf, wheat streak mosaic, potato tuber necrotic ringspot, faba bean necrotic yellows, pepino mosaic, tomato brown rugose fruit, and cucumber green mottle mosaic). Most examples involve long-distance virus dispersal, albeit inadvertent, by international trade in seed or planting material. With every example, the factors responsible for its development, geographical distribution and global importance are explained. Finally, an overall explanation is given of how to manage global virus disease pandemics and epidemics effectively.

Keywords: crop failure; crop losses; devastation; developing countries; disease; dissemination; domestication centers; epidemics; evolution; food insecurity; germplasm distribution; global; integrated disease management; international trade; pandemics; threat; virus.

Figure 1

(A) East African smallholder maize crop devastated by maize lethal necrosis disease (all maize plants killed or dying); potato understory crop unaffected. (B) Maize plant dying from maize lethal necrosis disease (center), surrounding maize plants healthy, image modified from [9]. (C) Wheat crop containing yellow dwarf diseased plants showing flag leaf symptoms of reddening and chlorosis. (D) Rows of wheat plants showing severe yellow dwarf disease symptoms of leaf chlorosis and reddening and plant stunting. (E) Wheat crop devastated by wheat streak mosaic disease showing plants with severe leaf chlorosis, deformation and necrosis, and overall plant stunting. (F) Close up of wheat plant showing wheat streak mosaic disease leaf symptoms of chlorotic yellowing and green streaking.

Figure 2

(A) Tuber of potato cultivar Nadine showing potato tuber necrotic ringspot disease (sunken necrotic rings and lines) typical of infection with R2 recombinant necrogenic strains of potato virus Y. (B) Sweet potato plant with sweet potato disease showing severe plant stunting and leaf chlorosis symptoms on right, healthy plant on left (image credit @International Potato Center/Segundo Fuentes). (C) Banana plantation with banana bunchy top diseased plants showing severe stunting, and short narrow upright leaves bunched at their tops, tall healthy plants on left side (image credit @International Institute of Tropical Agriculture/Lava Kumar). (D). Plum orchard showing premature fruit drop caused by plum pox disease. (E) Diseased fruit on plum tree showing ‘pock marks’ caused by plum pox disease. (F) Diseased apricot fruit harvested from apricot orchard showing ‘pock marks’ and internal flesh browning caused by plum pox disease. (G) Diseased apricot fruits splitting before harvest on plum pox diseased tree.

Figure 3

(A) Tomato brown rugose fruit diseased tomato fruit showing symptoms of uneven ripening with yellow and brown surface blotching (image credit @Volcani Center/Aviv Dombrovsky). (B) Pepino mosaic diseased tomato fruits infected with a severe pepino mosaic virus strain showing surface yellow marbling and discoloration (image credit @Dutch National Plant Protection Organization/Marlene Botermans). (C) Harvested tomato fruits showing severe yellow marbling symptoms that developed when initial infection with tomato brown rugose fruit mosaic virus was followed by later infection with a pepino mosaic virus mild strain commonly used commercially to provide cross protection against its severe strains (image credit @Volcani Center/Aviv Dombrovsky). (D) Cucumber plants growing in tunnel house: plants on right show symptoms of cucumber green mottle mosaic disease (chlorotic mosaic on leaves and plant stunting), plants on upper left are vigorous and healthy (insert shows early infected plant with severe stunting, reduction in leaf size and chlorotic mosaic). (E) Cucumber fruits with chlorotic mottle caused by cucumber green mottle mosaic disease (image credit @Volcani Center/Aviv Dombrovsky). (F) Fruits of honeydew melon with chlorotic mottle (left) and rockmelon with yellow mottle (right) caused by cucumber green mottle mosaic disease (image credit @Volcani Center/Aviv Dombrovsky). (G) Watermelon fruit with cucumber green mottle mosaic disease showing yellow spongy flesh and stem with necrotic lesions (image credit @Volcani Center/Aviv Dombrovsky. Images (E–G) all modified from [39].

Figure 4

Global spread of pepino mosaic virus after its first detection in Peru, South America in 1974 (red arrow). After a 25 year delay, it reappeared in Western Europe, North America and East Asia. During the following decade, it spread rapidly within Europe and North America, arrived in some Middle Eastern and African countries, and was detected in two countries neighboring Peru. Subsequently, the only spread recorded was within China. The virus, which is seed-borne, was spread inadvertently by the international seed trade. An subsequent focus on trade in heathy tomato seed stocks reduced the risk of further global spread (figure credit @Washington State University/Naidu Rayapati). Figure from Supplementary data in [9].

Figure 5

(A) Global spread of cucumber green mottle mosaic virus after its first detection in England in 1935. Colored circles show first detections within individual countries over three eras: yellow = 1935–1985; red = 1986–2006; blue = 2007–2016. This virus is readily seed-borne and was disseminated between continents, and across regions and countries, inadvertently, by the international cucurbit seed trade (figure credit @Volcani Center/Aviv Drombovsky). Figure modified from [39]. (B) Global spread of zucchini yellow mosaic virus after its first detection in Italy in 1973 (red arrow). During the following decade, it appeared in all continents with tropical, subtropical, Mediterranean, and temperate climates. It is seed-borne and was inadvertently disseminated between continents, and across regions and countries. This dissemination occurred mostly by the international cucurbit seed trade, but less often by infective aphid vectors blown in wind currents or international trade in infected fruit. The figure shows countries, and in some instances states within countries, reporting infection up to 2018 (figure credit @Washington State University/Naidu Rayapati). Figure from Supplementary data in [9].

Figure 5

(A) Global spread of cucumber green mottle mosaic virus after its first detection in England in 1935. Colored circles show first detections within individual countries over three eras: yellow = 1935–1985; red = 1986–2006; blue = 2007–2016. This virus is readily seed-borne and was disseminated between continents, and across regions and countries, inadvertently, by the international cucurbit seed trade (figure credit @Volcani Center/Aviv Drombovsky). Figure modified from [39]. (B) Global spread of zucchini yellow mosaic virus after its first detection in Italy in 1973 (red arrow). During the following decade, it appeared in all continents with tropical, subtropical, Mediterranean, and temperate climates. It is seed-borne and was inadvertently disseminated between continents, and across regions and countries. This dissemination occurred mostly by the international cucurbit seed trade, but less often by infective aphid vectors blown in wind currents or international trade in infected fruit. The figure shows countries, and in some instances states within countries, reporting infection up to 2018 (figure credit @Washington State University/Naidu Rayapati). Figure from Supplementary data in [9].