1. hibino 1996 rice viruses

July 10, 1996 17:9 Annual Reviews HIBINO.TXT AR14-14

Annu. Rev. Phytopathol. 1996. 34:249–74Copyright c© 1996 by Annual Reviews Inc. All rights reserved

BIOLOGY AND EPIDEMIOLOGYOF RICE VIRUSES

Hiroyuki HibinoChugoku National Agricultural Experiment Station, Nishifukatsu 6-12-1, Fukuyama,721 Japan

KEY WORDS: rice viruses, biology, transmission, infection cycle, epidemiology

ABSTRACT

The 15 known viruses that occur in rice are rice black-streaked dwarf, rice bunchystunt, rice dwarf, rice gall dwarf, rice giallume, rice grassy stunt, rice hoja blanca,rice necrosis mosaic, rice ragged stunt, rice stripe necrosis, rice stripe, rice tran-sitory yellowing, rice tungro bacilliform, rice tungro spherical, and rice yellowmottle viruses. This paper describes their geographical distribution, relation tovectors, infection cycles, field dispersal, and development, and lists recorded out-breaks of the viruses. Many rice viruses have become serious problems sincerice cultivation has been intensified. Double-cropping of rice using improved,photo-insensitive cultivars of short growth duration has significantly influencedthe incidence of these viruses.

INTRODUCTION

Rice,Oryza sativaL., is one of the most important cereal crops, with an annualproduction of 540 m tons in an area of 150 m hectares. About 92% of the world’srice production comes from Asia, where the grain is consumed directly as a foodand supplies about 36% of human total calorie consumption, compared to 20%worldwide. Rice has its origin in tropical semiaquatic grasses and is cultivatedin diverse environments: in flooded fields, uplands, deep water areas, and tidalwetlands; in lowlands and highlands; in tropical and in temperate regions, to53◦N.

Of the 15 viruses known to affect rice (57, 95, 118), 12 occur in Asia, 2 inAfrica, 1 in Europe, and 1 in the American continent. In major rice-growingcountries, rice virus diseases have occurred one after another and have inflicted

2490066-4286/96/0901-0249$08.00

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250 HIBINO

damage over a huge hectarage. The first major outbreak of rice viruses wasrecorded in Japan in 1897 for rice dwarf virus (RDV), followed in 1903 for ricestripe virus (RSV). From the mid-1950s to 1980s, other virus diseases have beenidentified as posing serious threats to stable rice production. In many countries,virus disease problems seem to have been accentuated by the introduction ofmodern agricultural techniques, requiring intensive cultivation and resulting ingreatly increased yields (10). The rice viruses may well have been present, butrarely reached epidemic proportions under traditional cropping when averagerice yield was low.

BIOLOGY AND EPIDEMIOLOGY

Rice Black-Streaked Dwarf VirusRice black-streaked dwarf virus (RBSDV) (128, 142) is a member of the fi-jivirus group of the family Reoviridae. The virus particles are polyhedral, about80 nm in diameter, and have 10 dsRNA segments and 5 proteins. Infected riceplants show pronounced stunting, darkening of leaves, twisting of leaf tips,splitting of the leaf margin, and waxy white-to-black galls along the veins onthe underside of leaf blades and the outer surface of sheaths and columns. Thegalls result from hyperplasia and hypertrophy of the phloem tissues. RBSDVis localized in the phloem and gall tissues.

RBSDV is transmitted in a persistent manner primarily by the planthop-per,Laodelphax striatellusand two other planthopper species (57, 128). It ispropagative in the vectors but is not transmitted via eggs. In infected rice andplanthopper cells, RBSDV particles are aggregated in or around viroplasmicinclusions or arranged in tubules in the cytoplasm of both types of cells.

RBSDV naturally infects rice, maize, wheat, barley,Alopecurus aequalisSobal, and some other weeds. After the rice or maize is harvested in RBSDVendemic areas, RBSDV-infectiveL. striatellusmoves to grass weeds and thento barley and wheat, where it transmits the virus and oviposits (71, 90, 112,124). The nymphs appear in September to October and overwinter as diapaus-ing nymphs at the fourth instar. Symptoms develop on RBSDV-infectedA.aequalis, barley, and wheat plants in March, or from November to December.Adults of the overwintered generation generally stay on the winter cereals andoviposit. The following (first) generation acquires the virus on infected plants,and moves to newly planted rice or maize in late May to June. It increasesgreatly its number in rice but not in maize, which is not a good host ofL.striatellus. Many first-generation adults are macropterous and are capable offlying long distances. Adults of the second and the third generations move fromthe early rice to late-planted rice and disperse RBSDV. In single-cropping rice

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EPIDEMIOLOGY OF RICE VIRUSES 251

areas, RBSDV incidence is generally high in early planted rice (71), whereasin double-cropping areas, it is high in the second rice crop or late-planted rice(124). Thus, RBSDV overwinters inL. striatellusnymphs, and also in wheat,barley, or weeds, on which the first generationL. striatellusacquires the virusand disperses it in rice and maize fields (71, 91, 112, 124). The incidence ofRBSDV is generally higher along the irrigation canals around rice fields (90,119). Application of high nitrogen fertilizer results in increases of the incidenceand severity of disease (71, 90, 119).

RBSDV occurs in China, Japan, and Korea. The first major outbreaks ofRBSDV in Japan was recorded in maize in the years 1957–1961, and in riceand maize in 1965–1967. In China, an outbreak occurred in 1963 and in 1965–1967 in rice, maize, wheat, and barley. The incidence of RBSDV was highin 1975–1976 in Korea (90). Except for these periods of high incidence, theoccurrence of RBSDV was local, and the incidence was generally low in allthree countries. RBSDV frequently caused severe damage in maize but lesserdamage in rice, or vice versa, in the same locations. In Tohoku, in northernJapan, RBSDV affects maize but not rice. In one locality in Hokkaido, northof Tohoku, it occurs in rice, although the incidence is low.

The high RBSDV incidence in Japan coincides with the period when thearea planted for early rice increased. The decreased incidence after 1968 is duelargely to a decline in the area planted for wheat and barley. The outbreak in1963 to 1967 in China was attributed to increased wheat cultivation (143). Thedecrease in the incidence in China after 1970 was attributed to the promotionof double and triple cropping of rice, which resulted in a reduction of areasplanted for wheat. That the major outbreaks of RBSDV occurred at about thesame time in Japan and China indicates a possible correlation between them.The vectorL. striatellusmigrates from southern China to Japan and may alsomove in the opposite direction, although the annual migration is limited (85).

Rice Bunchy Stunt VirusRice bunchy stunt virus (RBSV) (93, 146) is a possible member of the phy-toreovirus group. The virus particles are polyhedral, about 60 nm in diameter,and have 12 segments of dsRNA. Infected rice plants show stunting, increasedtillering, and short and/or narrow leaves.

RBSV is transmitted in a persistent manner byNephotettix cincticepsandN. virescens(16, 146). It is propagative in the vectors but is not transmittedvia eggs.

Rice is the only known host of RBSV. In Fujian, China (144, 149),N. cinc-ticepsandN. virescensthat acquire RBSV on late-planted rice plants stay onratooned rice or on grass weeds, overwinter at the nymph or adult stages, and dis-perse the virus to nursery beds or newly planted rice fields in early spring (149).

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252 HIBINO

Some RBSV-infected ratoons also overwinter and develop new leaves that serveas a virus source for the early planted rice. The incidence of RBSV is generallyhigher in the second crop rice, and is also higher at the edges of fields (144).

RBSV has been reported in Fujian, Gaundong, Guanxi, Hubei, Hunan,Jiangxi, Queichou, and Yunnan in China (148). A survey during 1976–1981found that the incidence in these locations was generally low and often nil.Average incidence was higher in 1979 than in other years.

Rice Dwarf VirusRice dwarf virus (RDV) (66, 142) is a member of phytoreovirus group ofthe family Reoviridae. The virus particles are polyhedral, about 70 nm indiameter, and have 12 segments of dsRNA and 7 proteins, one of which isserologically cross-reactive with the corresponding protein of rice gall dwarfvirus. Infected rice plants show pronounced stunting, increased tillering, andshort leaves that are darker green in color and with fine chlorotic specks. RDVis distributed in vascular bundles and in parenchymatous cells in the portions ofleaves that correspond to the white specks. Infected cells contain large roundor oval inclusion bodies in the cytoplasm. The bodies consist of a viroplasmicmatrix and numerous virus particles. Tubules enclosing virus particles andparacrystalline bodies occur in or around the bodies (H Hibino, unpublishedobservation). Starch accumulates in infected rice tissues.

RDV is transmitted in a persistent manner byNephotettix cincticeps, N. ni-gropictus, Recilia dorsalis,and some otherNephotettixspp. (57, 66). N.cincticepsis the most significant vector. RDV is propagative in the vectorsand transmitted from female adults to their progeny via eggs. RDV-infectedN.cincticepshas lower fecundity, higher nymphal mortality, and shorter longevity(105, 109). The vector ability of populations ofN. cincticepsvaried location-ally. In infected vector cells, RDV particles occur in or around viroplasmicinclusions, in phagocytic vesicles, or in tubules in the cytoplasm. Virus parti-cles occur in mycetocytes in close association with symbiotic organisms thatare transmitted via eggs (110).

RDV naturally infects rice and a few grass weeds. The weed hosts areprobably not important reservoirs of the virus (70, 129). After the late-plantedrice is harvested, infectiveN. cincticepsmove to grass weeds and overwinter asnymphal diapauses (67, 70, 82, 91, 106). Adults of the overwintered generationappear in March or April, and stay generally on weeds. In warm areas whererice is planted in early April or May, some leafhoppers move to rice and spreadthe virus. The first-generation adults, which are congenitally infected withRDV, appear in June and move to newly planted rice fields.

The population ofN. cincticepsdecreases during the winter season, remainsat a low level in the first generation, and increases rapidly after it moves into

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rice fields. The percentage of infectiveN. cincticepsin the populations is highin areas where RDV incidence is high. The percentage also changes dependingon cropping patterns and seasons. It is higher in the first than subsequentgenerations in areas where rice is planted early, but it is lower in the first andsecond generation in areas of medium and late rice (106). These changes wereattributable to lower fecundity and shorter life span of RDV-infected females,especially at high temperature (105, 109).

In rice double-cropping areas in China, the second- and the third-generationadults, which are infective, disperse RDV from the first- to second-crop rice(20, 21, 91). The incidence of RDV is generally higher in the second thanin the first crop. The incidence in the second-crop rice is correlated with thepercentage of RDV carriers in the overwintering generation (91), and with thepercentage and density of RDV carriers in the second generation (17). Thepopulation ofN. cincticepsdeclines to a low level during the winter season andincreases from generation to generation after the start of the rice season (91).

RDV incidence is generally higher at the edge of fields. Application ofexcess nitrogen fertilizer results in an increase of the vector population and thesusceptibility of rice plants to RDV, with a consequent increase in incidence ofthe virus (71). Epidemiological models of RDV have been developed in Japan(102, 104) and models for second-crop rice in China (17, 144).

RDV occurs in China, Japan, Korea, and Nepal, and was recently reportedin Mindanao, the Philippines (12). In southern and central Japan, high localincidence of RDV was recorded from time to time during the period 1889–1930.After 1955, however, the incidence of RDV reached epidemic proportions firstin southern Japan, then in central Japan (81). The incidence was especially highfrom 1967 to 1978 and declined thereafter. In Chejiang, China, the incidencewas high from 1969–1973 (91). The epidemic in Japan that started around 1955was correlated with the increase in areas planted for early rice, which allowed thefirst generation ofN. cincticepsto multiply and to disperse the virus in rice, andwhich raised vector density and the proportion of vectors that were infected withthe virus. The spread of the epidemic even farther after 1967 was attributable toseveral interconnecting factors: Cropping of winter wheat and barley in paddyfields decreased steadily after 1955; this in turn increased the number of ricefields left fallow during the winter season and favored the overwintering ofN.cincticepson weeds; meanwhile, vector populations developed resistance topesticide (81, 107). The decreased incidence of RDV after 1979 was attributedto the application of insecticide to rice seedlings in nursery boxes for machinetransplanters and to the plowing of fallow rice fields in winter or early spring.

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254 HIBINO

Rice Gall Dwarf VirusRice gall dwarf virus (RGDV) is a member of phytoreovirus group of thefamily Reoviridae (115, 142). The virus particles are polyhedral, about 65 nmin diameter, and have 12 segments of dsRNA and 7 proteins, one of which isserologically cross-reactive with the corresponding protein of RDV. Infectedrice plants show pronounced stunting, a reduced number of tillers, short darkergreen leaves, and small galls along the leaf veins on the under surface of leavesand the outer surface of sheaths. The galls result from hyperplasia and hy-pertrophy of the phloem tissues. In infected plants, RGDV is localized in thephloem and gall tissues. In infected plant cells, RGDV particles are aggregatedor scattered in or around viroplasmic inclusions, or arranged in tubules in thecytoplasm.

RGDV is transmitted in a persistent manner byN. cincticeps, N. nigropictus,Recilia dorsalis, and some otherNephotettixspp. (57, 115). RGDV is prop-agative in the vectors and is transmitted from female adults to their progenyvia eggs. In infectedN. cincticepscells, virus particles are packed in phago-cytic vesicles, or scattered in association with bundles of microfilaments or inviroplasmic matrix in the cytoplasm.

RGDV naturally infects rice and the grass weedAlopecurus aequalis(150).In southern China, RGDV-infected ratoons and volunteer rice plants over-winter and provide a reservoir of virus inoculum in the spring (150). Also,RGDV-infectedA. aequalisand leafhopper vectors overwinter and serve asvirus sources. The percentage of RGDV-infective leafhoppers in overwinteredpopulations is higher forR. dorsalisthan for other vectors.

RGDV occurs in Fujian and Guandong, China (148), in Malaysia, andin Thailand (115). An outbreak of RGDV occurred in the western part ofGuandong in 1981–1982 (150). The areas affected reached 7000 ha in 1981and 33,000 ha in 1982, and the yield loss was estimated at 2400 kg/ha in mod-erately affected fields and 4500 kg/ha in severe cases. RGDV incidence hasbeen low since 1983. In Thailand, RGDV is generally sporadic and causes onlyincidental reduction in yields.

Rice Giallume VirusRice giallume virus (RGV) is a strain of barley yellow dwarf luteovirus (9,116). The virus particles are polyhedral, about 25–28 nm in diameter, andhave a single molecule of ssRNA and a single protein. RGV-infected riceplants show stunting, reduced tillering, and yellow-to-orange discoloration ofleaves. Infected plants may die prematurely. In infected rice plants, RGVparticles are localized in the phloem tissues. In infected rice cells, virus particlesare scattered or aggregated in the cytoplasm. Infected cells contain double-

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membraned vesicles with fibrils, degenerated mitochondria, and deposits ofopaque materials along the cell wall.

RGV is transmitted in a persistent manner byRhopalosiphum padiand someother aphids (116). RGV is likely nonpropagative, but is circulative in thevectors.

RGV naturally infects rice and some cereals and grass weeds, includingLeersia orizoides(L) Sw (1, 2, 117), which is a common perennial grass in andaround rice fields and which also serves as a host ofR. padiin the absence ofrice. RGV overwinters inL. orizoides. In rice fields,L. orizoidesdevelops newleaves before rice seedlings start to grow and attractsR. padi(117). Giallume-diseased plants often appear in patches in the fields. These foci of infectedplants are associated with RGV-infectedL. orizoidesin the fields.

Barley yellow dwarf virus is distributed worldwide, but infection of rice bystrains of the virus has not been reported outside of northern Italy and Spain(116).

Rice Grassy Stunt VirusRice grassy stunt virus (RGSV) is a member of the tenuivirus group (56, 139).The virus particles are circular filaments, 6–8 nm in width, with possibly fourssRNA molecules with plus and minus polarities, and coat protein and RNApolymerase. RGSV is serologically distantly related to RSV. RGSV-infectedrice plants show pronounced stunting and proliferation of short, erect, and nar-row leaves that are pale green or pale yellow in color. Infected leaves may showmottling symptoms. RGSV strains that cause yellow-orange leaf discolorationand premature death of plants were detected in 1977 in Taiwan (13), in 1982–1983 in the Philippines and Thailand (59), and in 1984 in India (100). Thesevere strain that occurred in Taiwan was called rice wilted stunt virus. RGSV-infected plants produce a virus-specific protein that is serologically related to asimilar protein produced in RSV-infected plants. RGSV-infected rice cells con-tain masses of fibrils in the nuclei and cytoplasm and membrane-bound bodieswith fibrils in the cytoplasm. Tubules associated with isometric particles, 18 to25 nm in diameter, can be seen in the sieve tubes.

RGSV is transmitted in a persistent manner by the brown planthopperNila-parvata lugensand by two otherNilaparvataspp. (56, 57). It is propagative inthe vectors but is not transmitted via eggs.N. lugens,one of the most importantpests of rice in Asia, causes feeding damage or “hopper barn.” Average lifespanand fecundity are lower in RGSV-infective than in virus-freeN. lugens(64, 96).Populations ofN. lugensin which RGSV-transmission ability is low can be se-lected by mating noninfective hoppers (73). Isometric particles similar to thosefound in infected rice tissues are found in crystalline arrays in the fat body andtracheas of infectedN. lugens.

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RGSV naturally infects only rice. The vectorN. lugensis monophagousto rice. It flies from grassy stunt–affected fields to newly planted rice fields indistant areas and disperses RGSV and anotherN. lugens-borne virus, rice raggedstunt virus. In the tropics, RGSV andN. lugensare generally endemic in areaswhere rice is planted year-round. In cooler areas where rice is not planted duringthe winter season,N. lugensmigrates annually during the monsoon season fromthe endemic areas (19, 84, 89, 108). Some of the migrant planthoppers, whichtravel enormous distances over sea, carry RGSV (63, 74). Infected rice stubbleand volunteer rice plants also serve as a source of the virus. When the incidenceof RGSV is high, the rice crop also suffers direct damage from feeding byN.lugens, and in addition from rice ragged stunt virus.

Rice cultivars with resistance toN. lugenshave been planted widely in Asia.Incidence of RGSV is low to nonexistent in these resistant cultivars. However,populations ofN. lugens(biotypes) that can overcome the resistance have devel-oped a few or several years after release of the cultivars (26). Once populationsof N. lugensdeveloped that could feed and colonize in cultivars possessing aresistance gene, the cultivars showed no more resistance to RGSV in the fieldsand became subject to severe grassy stunt. In the Asian tropics, there had beenwidespread use of rice cultivars with a resistance gene to RGSV introduced froma line of the wild rice,Oryza nivara(80). The severe strain of RGSV (RGSV-2)that occurred in the Philippines was highly pathogenic to the resistant cultivars(59).

RGSV occurs in south and southeastern Asia, China, Japan, and Taiwan.RGSV incidence was high from 1970–1977 in Indonesia; from 1973–1977and in 1982–1983 in the Philippines (57, 59); in 1973–1974 and in 1981 inKerala, India (88); in 1972 and 1984 in Tamil Nadu, India (100); and in 1978in Kyushu, Japan (75). Since 1984, the incidence of RGSV has been generallylow in Asia. Although not well documented, the low incidence is thought tobe due to a change in virus transmission ability ofN. lugenspopulations. Inthe Philippines, the proportion of RGSV transmitters in populations that havefed on RGSV source plants ranged from 3 to 50% before 1977 (96), but from0–15% in 1984 (64; H Hibino, unpublished observation).

Rice Hoja Blanca VirusRice hoja blanca virus (RHBV) is a member of the tenuivirus group (103).The virus particles are filamentous, 3 nm in width, and have possibly fourssRNA strands of plus and minus polarities and coat protein. RHBV-infectedrice plants show stunting, chlorotic or yellow striping and mottling of leaves,and premature wilting. Rice cells infected with RHBV contain large massesof fine filaments, 8–10 nm in width, in the nuclei and cytoplasm. Infectedplants produce a large amount of virus-specific proteins. RHBV is serologicallyrelated toEchynochloahoja blanca virus species but not to other members of the

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tenuivirus group. The virus-specific protein of RHBV is serologically relatedto the similar protein inEchynochloahoja blanca virus–infected plants.

RHBV is transmitted in a persistent manner bySogatodes orizicola(Muir)(103). Sogatodes cubanusis capable of transmitting the virus from rice totheir grass hosts but not from rice to rice, which is not a host ofS. cubanus(31, 45). RHBV is propagative in the vectors and is transmitted at a highrate from female adults to their progeny via eggs. The percentage of infectiveplanthoppers in colonies can be increased to 90–100% by selective breeding(46, 51). S. orizicolawith newly acquired RHBV becomes infective after anincubation period of 30–36 days (44). Because of the long incubation periodof the virus inS. orizicola, planthoppers that acquire RHBV through feedingon infected plants rarely live long enough to transmit the virus.S. orizicolainfected with RHBV have a shortened life span, low fecundity, and reducednymph viability (29, 76).

RHBV naturally infects only rice.S. orizicolacolonizes only on rice anda few wild rice species (27). RHBV is dispersed primarily byS. orizicolacongenitally infective of the virus.

RHBV occurs in Central and South America, in the Caribbean, and from1957–1959 in the southern United States (5). The first outbreak of RHBVoccurred in Latin America during the years 1956–1967. From 1965–1967,however, damage caused by the vector,S. orizicola,was more severe than thatcaused by the virus (76). The disease did not cause any serious economicproblems from 1968–1980, but when it reappeared in some Latin Americancountries from 1981–1985, it reached epidemic proportions (152).S. orizicolawas observed in 1957, 1959, and 1962 in rice growing areas of the southernUnited States (5).

In Latin American countries, rice hoja blanca, which occurred only sporadi-cally before 1957 (4), became important after the introduction and widespreadcultivation of new rice cultivars. There was a very large increase in sogata den-sity in western Cuba and Venezuela after the introduction of short-maturing ricevarieties that made multiple cropping possible (31). The cyclic nature of the hojablanca epidemic is explained by the deleterious effects of RHBV onS. orizicolaand the possible selection of virus noninfective populations (152). The plant-hopper’s ability to support replication of the virus is inherited, and susceptibilityto the virus in wild populations may be lowered after the outbreak of disease.

Rice Necrosis Mosaic VirusRice necrosis mosaic virus (RNMV) is a member of the bymovirus group of thefamily Potyviridae (40, 69). The virus particles are flexuous filaments, 205 and550 nm in length and 13–14 nm in width, and contain 2 ssRNA strands and a sin-gle protein. The virus is serologically related to barley yellow mosaic and wheatyellow mosaic viruses. RNMV-infected rice plants show moderate stunting;

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258 HIBINO

reduced number of tillers; a spreading growth habit; elongated or spindle-shaped, yellow flecks and streaks on the lower leaves; and necrotic flecks atthe basal portions of stems and sheaths. In infected rice cells, RNMV parti-cles are scattered or associate with laminated aggregates and pinwheels in thecytoplasm. Infected cells have complex membranous bodies in the cytoplasm.

RNMV is transmitted by the soilborne fungusPolymyxa graminis(40).Zoospores from zoosporangia or resting spores ofP. graminis that developin RNMV-infected root cells penetrate into the root cells of other plants andtransmit the virus. Two isolates of the virus, one from Japan and one foundat Cuttack, India, which are thought to be RNMV, were transmitted to rice bymechanical means (42, 47), but mechanical transmission of other RNMV iso-lates proved difficult (40). The Japanese isolate was transmitted from infectedplants to the next generation through seeds (41), but no seed transmission ofthe virus has been reported for other isolates (40). The two isolates have notbeen well characterized.

RNMV-affected soil (i.e. containingP. graminis) retains infectivity for manyyears (40). RNMV infection of rice seedlings through soil is high when the soilreaches a temperature of 25–30◦C and soil moisture is low. Because wet soil isnot favorable for infection, RNMV is rare in rice seeded directly into floodedfields. Rice necrosis mosaic occurred either in transplanted fields or in fieldsseeded directly and grown under an upland condition. In transplanted fields,rice necrosis mosaic occurs only when seedlings are infected with RNMV innurseries. Plant infection with RNMV after transplanting is rare. In Japan, afterthe introduction of machine transplanters using seedlings prepared in nurseryboxes, the incidence of RNMV declined rapidly and disappeared in most af-fected areas. Many upland rice cultivars in Japan have a high level of resistanceto the disease, and the incidence of RNMV is generally low in upland rice fields(40).

Rice necrosis mosaic was first recognized in 1959 in Okayama, Japan, andsubsequently during 1962–1970 in southwestern and central Japan (40). Asimilar disease occurred once only in Cuttack, India (47). All isolates of RNMVexcept the Indian isolate only infect rice naturally. The Indian isolate naturallyinfects weeds,Ludwigia perennisand Brachiaria ramosa(48). InfectedL.perennisshow increases in height, leaf size, and stem diameter (49). The roleof these weeds in the disease cycle is not known.

Rice Ragged Stunt VirusRice ragged stunt virus (RRSV) is a member of the oryzavirus group of thefamily Reoviridae (101, 142). The virus particles are polyhedral, about 50 nmin diameter, and contain 10 dsRNA strands and 5 major proteins. Infected riceplants show stunting, abnormal leaves with serrated edges or twisted tips, and

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vein swelling or galls on the underside of leaf blades and outer surface of theleaf sheaths. The gall results from hyperplasia and hypertrophy of the phloemtissue. Plants infected with RRSV at the seedling stage develop new leaveswith identifiable symptoms two weeks after inoculation and thereafter developleaves showing milder or no definite symptoms. At the heading stage, the plantsagain show symptoms on upper leaves and flag leaves. In infected plants, RRSVis localized in the phloem and gall tissues. Infected cells contain large inclusionbodies consisting of a viroplasmic matrix and numerous virus particles.

RRSV is transmitted in a persistent manner by the brown planthopper,Nila-parvata lugens, and anotherNilaparvataspp. (57, 101). It is propagative in thevectors but is not transmitted via eggs. In infected vector cells, RRSV particlesare aggregated in or around the viroplasmic inclusions or arranged in tubulesin the cytoplasm.

RRSV infects many graminaceous plants in inoculation tests usingN. lugens.Natural infection of weeds and cereals other than rice is rare or nonexistent,asN. lugensis monophagous to rice (53, 101). In the Asian tropics, RRSVand the brown planthopper are endemic in irrigated areas where rice is grownthroughout the year. RRSV-infected planthoppers are the primary source of thevirus. Macropterous adults ofN. lugensmove from RRSV-damaged fields tonewly planted rice fields and spread the virus.

As described for rice grassy stunt virus, rice cultivars possessing resistancegenes toN. lugenshave been planted widely in Asia. Resistant cultivars thatformerly had little or no ragged stunt had severe infestations when populationsof N. lugensdeveloped that were able to feed and colonize in these cultivars.

The occurrence of rice ragged stunt was first recognized in 1977 in Indonesia,Malaysia, the Philippines, and Thailand; in 1978, in China, India, Sri Lanka(53), and Taiwan (14); and in 1979, in Japan (131). The origin of RRSV isnot known. In many of these countries, RRSV soon reached epidemic levels:incidence was high in 1977–1981 in Indonesia and the Philippines, and in 1980–1982 and 1989–1990 in Thailand. Incidence has generally been low in manycountries since 1982, except in Thailand and Vietnam. RRSV may have longbeen present at a low level in many of these countries (97). In the Asian tropics,however, the population density of the vectorN. lugensincreased dramatically,and anotherN. lugens–borne RGSV reached epidemic proportions in manycountries in the 1970s (30). That RRSV was present but unnoticed for manyyears is unlikely given the severity of infestation with the vector (97). RRSVmay have been localized in an area where the vector population was relativelylow in the early 1970s. SinceN. lugensis capable of long-distance transoceanicflight (84), RRSV might have been dispersed during 1977–1979 from localizedareas to other areas through long-distance flights byN. lugens.

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Rice Stripe Necrosis VirusRice stripe necrosis virus RSNV is a possible member of the furovirus group(36, 37). The virus particles are rod shaped, 120, 270, or 380 nm in length and 20nm in width. RSNV naturally infects only rice. Infected plants show stunting,reduced number of tillers, and chlorotic or yellow stripes on leaves, which laterbecome necrotic. In RSNV-infected cells, virus particles are aggregated in thecytoplasm. Paracrystalline inclusions occur in the cytoplasm of infected cells.

RSNV is soilborne and is maybe transmitted by the fungusPolymyxa grami-nis. However, it is also mechanically transmissible.

Rice stripe necrosis was first reported in the Ivory Coast in 1977 (99). Thedisease occurs in the Ivory Coast, Liberia, Nigeria, and Sierra Leone (37). Indisease-affected fields, stripe necrosis occurs erratically from season to season.Disease incidence in upland rice is higher when short periods of intermittentrain are interspersed with long dry periods at the beginning of the rainy season.In the fields, the disease appears in patches, which expand progressively.

Rice Stripe VirusRice stripe virus (RSV) is the type member of the tenuivirus group (138, 139).The virus particles are circular filaments 290, 510, 610, 840, or 2110 nm inlength and 9 nm in width. Virus particles contain five strands of ssRNA ofplus and minus polarities, coat protein, and RNA polymerase. RSV is sero-logically related to maize stripe virus and RGSV. Infected rice plants showchlorotic stripes or mottling and necrotic streaks on leaves, and premature wilt-ing. Chlorotic leaves are unfolded, and later droop and wilt. Infected plantsproduce relatively high concentrations of virus-specific proteins, which areserologically related to similar protein produced in RGSV-infected plants. In-fected rice cells contain large masses of granular or sandy structures in thecytoplasm and nuclei and masses of needlelike and paracrystalline structuresin the cytoplasm and vacuole.

RSV is transmitted in a persistent manner byLaodelphax striatellusandsome other planthoppers (57, 138). It is propagative in the vectors and trans-mitted from female adults to their progeny via eggs. The effects of RSV onL.striatellusare uncertain. Nasu (109) reported lower fecundity, higher nymphalmortality, and shorter life span inL. striatellusthat have been infected with RSV.Kishimoto (86) found no such adverse effects on the planthopper. The vectorability of L. striatellusis controlled genetically (83). Populations ofL. striatel-luswith low or high virus transmission (acquisition) ability can be obtained byselective breeding (83). RSV is mechanically transmissible, but with difficulty.

RSV naturally infects rice, wheat, barley, oat, foxtail millet, and some gram-inaceous weeds (138). These cereals, with the exception of rice and winterweeds, are not good hosts of RSV and do not serve as virus sources for the next

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crop season. After rice is harvested from September to October in central andsouthern Japan, infectiveL. striatellusmoves to grass weeds and then to wheatand barley where it transmits the virus and oviposits (23–25, 113, 141, 151).Nymphs appear in late September to October and overwinter as diapausingnymphs on wheat, barley, and grasses. In March, adults of the overwinteredgeneration appear, and some may move to early rice. The following (first) gen-eration is congenitally infective and prolific. From the end of May to mid-June,the first-generation adults, many of which are macropterous, move to newlyplanted rice fields and transmit the virus. The major infection of rice is incurredby the first-generation adults and the second-generation nymphs. Generally,virus incidence is low in rice fields planted very early in April, high in fieldsplanted in May, and lower again in fields planted later. Rice plants infected withthe virus at the early growth stage show severe symptoms and die prematurely.Plants exposed to infectiveL. striatellusat later growth stages had less infectionand showed milder symptoms and no wilting. In northern Japan (Hokkaido),RSV-infected adults of the overwintered generation appear from May to June,move to newly planted rice seedlings, and transmit the virus (78). In Japan, theincidence of RSV in the following crop season can be estimated by the densityand percentage of RSV carriers in the overwintering populations (86).

RSV occurs in China, Japan, Korea, Siberia, and Taiwan. In Japan, theincidence of RSV was very high from 1960–1972 and increased again from1977–1986 (81). In Korea, it was high during 1964–1965 and 1973–1974(23). In China, high incidence was recorded in 1964 in Shanghai and Jiangso,Zhejiang; in 1975–1976 in Beijing; in 1984 in Shandong; and repeatedly from1974–1990 in Yunnan (94). The increase during the 1960s in Japan was duelargely (1) to an increase in the areas planted to early maturing rice, whichprovides favorable conditions forL. striatellusand RSV, (2) to increased winterwheat and barley production, which supports a large planthopper populationduring the winter season, and (3) to staggered planting of early to late rice,which serves as a continuous source of virus-susceptible young seedlings (81).The decrease in incidence after 1973 was due to the decline in areas plantedfor winter wheat and barley that had started around 1960. In the late 1970s,the areas increased to some extent. The second epidemic in Japan started in1977 whenL. striatelluspopulations were very high in Kanto (central Japan). Inareas where RSV was epidemic, rice cultivars resistant to RSV were introducedin 1981, and as areas planted for the cultivars increased (111, 134), incidencedeclined to a low level in Kanto by 1988. RSV is endemic in localized areas incentral and western Japan.

Rice Transitory Yellowing VirusRice transitory yellowing virus (RTYV) is a member of the subgroup nucle-orhabdovirus of the plant rhabdovirus group (127). It is identical or very close

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to rice yellow stunt virus, which was identified at about the same time in China(35). Virus particles are bullet shaped, 180–210 nm in length, and 94 nm inwidth, and have ssRNA and 4 or 5 proteins. Rice plants infected with RTYVshow leaf yellowing, reduced tillering, and mild stunting. Later, infected plantsdevelop normal-looking leaves and may appear healthy, but symptoms mayreappear after this temporary recovery. In infected rice plants, RTYV is local-ized in the phloem tissues. A mass of RTYV particles appears between twonuclear membranes in infected cells.

RTYV is transmitted in a persistent manner byNephotettix cincticeps, N.nigropictus, andN. virescens(57, 127). It is propagative in the vectors butis not transmitted via eggs. Vector efficiency is high inN. cincticepsandN. nigropictus, but low in N. virescens.In infected leafhopper cells, RTYVparticles are found in vacuolate structures in the cytoplasm.

RTYV naturally infects only rice. After the harvest of late-planted rice,RTYV overwinters in rice stubble or in the vector,N. cincticeps. N. nicropictuslives on weeds, and its density is generally low in rice.N. nigropictusandweed hosts may play a role in the infection cycle of RTYV in hillside areas.Overwintering hosts of the virus are rice stubble in southern China (33), inN.cincticepsand occasionally in rice stubble in Fujian, China, and Taiwan (15,142), and inN. cincticepsin the middle and lower basin of the Yangtze River,where rice stubble is unable to overwinter (18, 91). After early planted riceis harvested, second- or third-generation adults ofN. cincticepsmove to thelate-planted rice and spread the disease.

The incidence of RTYV is generally low in the first rice crop and high inthe second crop (15, 17). Under epidemic conditions, the incidence of RTYVin the second crop is correlated to the rate of RTYV-infectiveN. cincticepsinthe population,N. cincticepsdensity, and winter temperatures (15, 17, 18, 92)and to virus incidence in early rice and the rate of infective leafhoppers in thepopulation in June (145). RTYV and RDV, which have common vectors,N.cincticepsandN. nigropictus, frequently occur together in southern and centralChina (17, 91, 145).

RTYV occurs in southern and central China, the Nansei Islands (Okinawa)of Japan, Taiwan, and Thailand (57). Rice yellow stunt virus has been reportedin Vietnam (140) and Laos (126). Major outbreaks of RTYV occurred in 1960–1962, 1973–1975, and 1977–1980 in Taiwan (15, 22, 133); in 1964–1966 andin 1979 in Guandong, China (33); in 1966, 1969, and 1973 in Fujian (145);and in 1970–1972 in Cheijang (18). The incidence has generally been lowsince the mid-1980s. In 1979, RTYV was found in Chiengrai and Chienmai,Thailand (68). Areas affected were localized, and its incidence is generally lowin Thailand.

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Rice Tungro Bacilliform and Rice Tungro Spherical VirusesTungro (4, 58) is the most important virus disease of rice in the Asian tropics. Itis a composite disease caused by rice tungro bacilliform virus (RTBV) and ricetungro spherical virus (RTSV). RTBV is a member of the badnavirus group.Virus particles are bacilliform, 100–300 nm in length and 30–35 nm in width.RTBV has a circular dsDNA and a single protein. RTSV is a member of theribotungrovirus group. Virus particles are polyhedral, about 30 nm in diameter.RTSV has ssRNA and three proteins.

Rice plants infected with RTBV and RTSV together show tungro symptoms,including stunting, yellow or yellow-orange discoloration, and reduced tillering(61). Discolored leaves may show irregularly shaped dark-brown blotches.The leaves, especially the younger ones, may show striping or mottling andintervernal chlorosis. Plants infected with RTBV alone show similar but mildertungro symptoms. Plants infected with RTSV alone show no obvious symptomsexcept very mild stunting. In infected plants, RTBV is localized in the vascularbundles and RTSV in the phloem tissues (132). In infected cells, both RTBV andRTSV particles are scattered or aggregated in the cytoplasm. RTSV particlesalso occur in vacuoles. Viroplasm-like inclusions and membraneous massesoccur in the cytoplasm of RTSV-infected cells.

RTBV and RTSV are transmitted in a semipersistent manner byNephotet-tix virescens, N. nigropictus, N. cincticeps, Recilia dorsalis, and some otherNephotettixspp.N. virescensis the most efficient vector of tungro disease (54,62, 79).N. cincticepsis the principal vector of rice waika virus (RTSV) in Japanand probably serves as the vector of tungro in southern China.N. nigropictusandR. dorsalisare less efficient vectors of RTBV and RTSV. Immediately afterfeeding on source plants infected with RTBV and RTSV, the vector leafhoppertransmits the viruses, either both viruses together or RTBV or RTSV alone. Itretains RTBV for 4–5 days and RTSV for 2–4 days. The leafhopper readily ac-quires RTSV on source plants infected with RTSV alone, but it does not acquireRTBV on plants infected with RTBV alone (61). Leafhoppers that have fedpreviously on RTSV-infected plants acquire RTBV from plants infected withRTBV. Through feeding on plants infected with RTBV, the leafhopper gains ahelper component and thus the ability to acquire RTBV. The leafhopper retainsthe helper activity for the acquisition of RTBV for seven days. After feedingon antiserum to RTSV, the leafhopper loses RTSV infectivity but retains thehelper activity (60). After molting, leafhoppers lose both RTBV and RTSVinfectivity (67, 95), as well as the helper activity (11). RTSV is unlikely to bea bearer of the helper activity. The helper component may be a protein codedon the RTSV genome and produced in RTSV-infected cells, similar to those forpotyviruses and caulimoviruses (120). Both RTBV and RTSV are stylet-borne,

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and the helper component may be essential for specific adsorption of RTBV onthe leafhopper’s mouth wall. The helper component has not been isolated fromplants infected with RTSV. The helper gene has not been located on the RTSVgenome.

N. virescensis monophagous to rice, and its density can reach high levels de-pending on the environment. After rice is harvested, the density ofN. virescensfalls rapidly to a low level or to nil in the rice fields. Rice is likely the only hostof RTBV and RTSV, although all wild rice tested thus far and perhaps someweeds also can be infected with RTBV and/or RTSV by exposing to RTBV+ RTSV or RTSV-infectiveN. virescens(3, 79, 87). Tungro-infected plantsincluding rice stubble or volunteer rice serve as sources of RTBV and RTSV.N. virescensthat feeds on source plants moves to newly transplanted fields insurrounding areas (136) and disperses the viruses. Although the flying abilityof N. virescensis not known, its range is suspected to be several kilometers ormore. In Kyushu, Japan, rice stubble infected with rice waika virus overwintersand develops new leaves in spring, which serve as the source of the virus (72).

Tungro-infectiveN. virescenslands on newly planted rice fields, transmitsthe viruses to one or more rice seedlings, which then serve as the source forfurther dispersal in the field. Generally, plants with secondary infection fromsuch sources form patches a few to several meters in diameter, which later fusewith each other. Generally, in tungro-endemic areas, major infection of riceplants with RTBV and RTSV occurs after transplanting, and the infection ratein seedbeds prepared in the field is low (137). In transplanted fields, infectionwith RTSV alone precedes infection with RTBV (137), as the source of RTSVis more prevalent in surrounding fields (6). RTSV is often spread alone as anindependent but a latent disease (6).

Tungro incidence is generally low in fields planted in the early crop seasonwhen the vector population is low, but it is high in fields planted later when thevector population is higher (125). Tungro incidence is not necessarily correlatedto vector density (4, 98), although vector density is much higher in epidemicthan in nonepidemic years.

In the Asian tropics, rice cultivars possessing resistance toN. virescenshavebeen used widely to control tungro disease (58). Many resistant cultivars thatformerly had a little or no tungro sustained severe damage several years afterthe release of the resistant cultivars because of the development of populationsof N. virescensable to feed and colonize on the cultivars (28, 58).

The practice of definite fallow periods after each crop season in each areahas been followed in Indonesia and Malaysia to solve the tungro problems.In South Sulawesi, Indonesia, an integrated tungro management scheme hasbeen successfully practiced since 1983 (125). In this scheme, rice planting was

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scheduled to have nearly synchronous growth and to maintain a definite fallowperiod after the harvest of each crop in each area, in addition to the deploy-ment (rotation) of cultivars with different resistance toN. virescens. Under thescheme, tungro incidence was zero or negligible when planting occurred onschedule or up to one month later, but it was high when planting occurred twoor three months later. Low tungro incidence under the management schemewas mainly attributable to the slow rate of increase in the vector population andto the absence or paucity of sources of tungro in the area.

Tungro disease occurs in south and southeastern Asia and in southern China(57, 147). RTSV alone (rice waika virus) was once epidemic in Kyushu, Japan(43, 130). The occurrence of RTSV alone has been reported in Shandong, Fubei,Funan, Fujian, Jiangxi, Guandong, and Hainan in China (148). Major outbreaksof tungro occurred in 1969 in Bangladesh; in 1969, 1984, and 1985 in India;from 1969–1971, 1972–1975, 1980, 1984–1985, and 1994–1995 in Indonesia;in 1969 and 1982–1983 in Malaysia; in 1957, 1970–1971, and 1983–1984 in thePhilippines; and from 1965 to 1970 in Thailand (57). As indicated above tungrohas become increasingly important since the mid-1960s, when planting of high-yielding cultivars was started in the Asian tropics and double-cropping of ricebecame common in irrigated areas. In most irrigated areas in the Asian tropics,rice plantings are staggered and crop seasons are indefinite. This condition isfavorable for tungro and the vectorN. virescens. Use of high-yielding cultivarswith similar genetic backgrounds over wide geographic areas also favored thedevelopment of populations of vectors adapted to the cultivars (28, 58).

An outbreak of rice waika virus (RTSV) occurred in 1971–1974 in Kyushu,Japan (43, 131). An abnormality similar to waika had been observed in ricein Kyushu since 1964. The high incidence of rice waika virus in 1971–1974was attributed to higher winter temperatures in 1972 and 1973 and to use of arice cultivar that is highly susceptible to the virus and that was planted widelyin Kyushu during this period. More waika-infected rice stubble overwintersin Kyushu if winter temperatures are higher (72). The incidence of waikadeclined to a low level and eventually disappeared in most places after 1975.The decline was attributed to low winter temperatures in 1974; replacementof the susceptible cultivar with nonsusceptible cultivars; and lower density ofN. cincticepsdue to insecticide application in seedling boxes and to intensifiedplowing of fallow rice fields (43, 130).

Rice Yellow Mottle VirusRice yellow mottle virus (RYMV) is a member of the sobemovirus group (7,8). The virus particles are polyhedral, about 30 nm in diameter, and containone molecule of ssRNA and one protein. Infected rice plants show mottlingor yellow-orange discoloration of leaves, stunting, and sterility. In infected

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rice cells, virus particles are scattered or aggregated in crystalline arrays in thecytoplasm. Infected cells contain long flexuous tubules, 10–15 nm in diameter,and aggregates of fibrils in the cytoplasm. Virus concentration is high in infectedrice tissues.

RYMV is transmitted in a semipersistent manner by a number of chrysomelidbeetles, includingSesselia pussilla, Chaetocnema pulla,andTrichispa sericea(7, 8). It is mechanically transmissible and can also be transmitted by the long-horned grasshopperConocephalus merumontanus. S. pussillais an efficientvector, whereasC. pullaandT. sericeaare less efficient but occur abundantlyin rice fields. RYMV is not circulative in the vector beetles, which retain thevirus for 1–8 days, with an average of 2–3 days.

RYMV naturally infects the wild speciesOryza longistaminatain Niger andMali (77), and perhaps elsewhere (39). In Nigeria, however, infection of thewild rice has not been confirmed (123). The role of the wild rice as the sourcefor spreading RYMV is not known. Four grasses,Dinebra retroflexa, Eleusineindica, Eragrostis tenuifolia, and anOryzaspecies, sustained an infection withRYMV when planted in rows alternatively with artificially infected rice plants(114).

RYMV occurs in irrigated paddies, inland swamps, deep-flooded rice, and inupland rice (121). The incidence is generally high in irrigated areas where morethan one crop of rice is planted. In such areas, infected rice stubble is the majorsource of RYMV. The virus spreads from the source to other plants mainly bymechanical means with the aid of harvesting stickers or through contacts viainjury, and also by vector beetles. As virus concentration is high in infectedtissues, incorporation of infected plants or their sap into soil or into flood waterfacilitates infection of newly transplanted seedlings. Yellow mottle–infectedplants appear two to three weeks after transplanting as patches along the edgesand in the field. The patches enlarge and may fuse with each other and eventuallycover a large area. The incidence of RYMV is generally high during the rainyseason. RYMV was first observed in Kenya in 1966, and subsequently, during1976 to 1983, was found in many rice-growing countries of Africa, includingBurkina Faso, Ghana, Ivory Coast, Kenya, Liberia, Mali, Niger, Nigeria, SierraLeone, and Tanzania. In 1989, it was found in Madagascar (122).

CONCLUSION

Many of the 15 rice viruses, especially planthopper- or leafhopper-borne viruses,have reached epidemic proportions in many countries and have caused seriousdamage in rice. Major outbreaks of the hopper-borne viruses were generallyassociated with high densities of their vectors. Although many virus diseaseshave not been well analyzed, a number of outbreaks were attributed to majorchanges in cultivation practices.

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For example, before 1950 in Japan, wheat and barley were planted in paddyfields during the winter season, and rice seedlings were raised in nursery bedsand transplanted in June or July after the winter cereals had been harvested. Un-der this cropping system, rice virus diseases, except rice dwarf and rice stripe,were not recognized as threats to rice production. RDV and RSV were endemicin localized areas of southern and central Japan and sometimes even reachedepidemic levels. Since 1950, major changes in rice cropping systems have hadan enormous impact on diseases and insect pests, especially on hopper-bornevirus diseases in rice (81). The changes included increased areas planted forearly season rice, which was transplanted in late April to May; reduction in ar-eas planted for the winter cereals from 1.8 million ha in 1950 to 0.9 in 1965 andto 0.2 in 1975; and the introduction of machine transplanters using seedlingsprepared in nursery boxes under a controlled environment. The early plantingincreased the probability of stable yields and decreased potential damage fromtyphoons. The reduction in growth of winter cereals was mainly due to in-creases in the cost of production, which increased the importation of low-pricecereals. The introduction of early rice and early planting of middle-season ricecreated a sequence of crops starting from late April, and provided a continu-ous source of young seedlings for the viruses and for the first and the secondgenerations of their vectorsN. cincticepsandL. striatellus. The application offertilizer increased substantially after 1950, producing conditions favorable forboth the viruses and their vectors. As a result, virus incidence, vector popula-tion, and the percentage of virus infective hoppers in overwintering populationsall increased dramatically (81). The conditions were also favorable for anotherL. striatellus-borne virus, RBSDV, and for aN. cincticeps-borne rice yellowdwarf phytoplasma (81). The epidemics of RSV and RDV, which are trans-mitted through eggs, lasted over ten years, but that of RBSDV and rice yellowdwarf phytoplasmas eased in three to four years. Epidemics where the virus istransmitted via vector eggs persist long after the environment has become lessfavorable for the virus and for its vector (86).

The introduction of machine transplanters also affected disease incidencein Japan. RNMV disappeared after their introduction. The use of nurseryboxes provided an effective control option for hopper-borne viruses, throughthe appplication of insecticides in the nursery. On the other hand, use of nurseryboxes facilitated the spread of certain seed-borne fungal and bacterial diseasesthat had not been serious problems in rice production hitherto (118).

In China, major outbreaks of rice viruses were recorded after 1963, whendouble-cropping of rice became common in southern China and total productionstarted to greatly increase (FAO Statistics). The outbreaks were attributed toincreased double-cropping and early planting of the first-crop rice, and to theapplication of fertilizers (143, 146). The epidemics of RBSDV in 1963–1967were attributable to increased wheat cultivation (143).

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In the Asian tropics, the first high-yielding semi-dwarf cultivar was bred atIRRI and released in the mid-1960s (52). High-yielding cultivars have subse-quently been planted widely in the Asian tropics and have been used as parentsin the rice breeding programs in many countries (50). Cultivar improvement hashad an enormous impact on Asian agriculture and has resulted in a remarkableincrease in rice yield and total rice production in Asia, especially in tropicalregions (38, 52). This change is known as “The Green Revolution.” Beforehigh-yielding cultivars were introduced, rice cultivars planted were tall, lowtillering, required short days for flowering, and needed a long period of growth(five or six months) to mature. The taller traditional rice lodged if nitrogenfertilizer was applied, and it was planted in the monsoon season. The high-yielding cultivars are short and photo-insensitive, have higher tillering ability,and a shorter growing season of four months. The use of improved cultivarsallows more than two crops a year to be planted, if sufficient irrigation is avail-able. Since the 1960s, double-cropping of rice has become popular in irrigatedareas and the application of fertilizer has increased greatly. As a result, riceplanting is staggered in irrigated areas, and rice exists all year round. Also,there is strong tendency for planting wide areas with rice cultivars having simi-lar genetic background. Such conditions are favorable to rice viruses and theirvectors. In the Asian tropics, many virus diseases and their vectors, not recog-nized previously as problems in rice production, have become major threats tothe stable production of rice.

In Latin America, the high incidence of RHBV was attributed to a large in-crease in the density of vectors after improved rice cultivars were introduced,which allowed double-cropping of rice (45). Although the pathogenic virus isnot hopper-borne, the incidence of RYMV in Africa is generally high in irri-gated areas where rice is planted year round (136). It is likely that RHBV andRYMV, which are indigenous in Latin America and Western Africa, respec-tively, have become serious pests after the introduction of the new rice cultivarsand intensification of rice-cropping systems (135).

Rice has a long history of cultivation in Asia, spanning from 2000 to 4000years. Many rice viruses have probably long been in the equilibrium stageestablished between host and pathogen in each area (136). This balance wasdisrupted by the recent intensification of cropping systems, including the in-troduction of double-cropping and the application of fertilizer, which greatlyincreased rice yield and total rice production in many countries. It would notbe practical to change the rice-cropping system extensively again to deal withproblems caused by viruses and other pests. Indeed, the level of productionachieved over the past three decades is still insufficient to support the burgeon-ing population, and it has to be increased even further. The development of

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ecologically sound management practices to deal with rice virus diseases in thedouble-cropping system is critical. Fortunately, in some countries in higherlatitudes in Asia, the incidence of virus diseases in rice has generally been lowfor over ten years, indicating the possible establishment of a new equilibriumbetween rice and pathogen. In the Asian tropics, management practices in-corporating a definite fallow period after each crop season in each area havebeen successful in managing rice tungro disease (125). In such areas, the tun-gro viruses are apparently endemic and do not cause economic losses. Moreresearch is needed on the epidemiology of rice viruses in relation to croppingsystems so that effective management strategies can be implemented.

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Annual Review of Phytopathology Volume 34, 1996

CONTENTSPLANT PATHOLOGY: A Discipline at a Crossroads, Albert R. Weinhold 1HELEN HART, REMARKABLE PLANT PATHOLOGIST (1900–1971), Roy D. Wilcoxson 13DR. GOTTHOLD STEINER (1886–1961): VERSATILE NEMATOLOGIST, Robert P. Esser 25THE RED QUEEN HYPOTHESIS AND PLANT/PATHOGEN INTERACTIONS, Keith Clay, Paula X. Kover 29THE ROLE OF PLANT CLINICS IN PLANT DISEASE DIAGNOSIS AND EDUCATION IN DEVELOPING COUNTRIES, Reuben Ausher, Israel S. Ben-Ze'ev, Robert Black 51DWARF BUNT: Politics, Identification, and Biology, D. E. Mathre 67FUNGAL TRANSMISSION OF PLANT VIRUSES, R. N. Campbell 87EPICHLOË SPECIES: Fungal Symbionts of Grasses, Christopher L. Schardl 109FASTIDIOUS XYLEM-LIMITED BACTERIAL PLANT PATHOGENS, Alexander H. Purcell, Donald L. Hopkins 131BACTERIAL AVIRULENCE GENES, Jan E. Leach, Frank F. White 153CHEMORECEPTION IN PLANT PARASITIC NEMATODES, Roland N. Perry 181NEMATODE MANAGEMENT IN SUSTAINABLE AND SUBSISTENCE AGRICULTURE, J. Bridge 201HELPER-DEPENDENT VECTOR TRANSMISSION OF PLANT VIRUSES, Thomas P. Pirone, Stéphane Blanc 227BIOLOGY AND EPIDEMIOLOGY OF RICE VIRUSES, Hiroyuki Hibino 249MOLECULAR BIOLOGY OF RICE TUNGRO VIRUSES, Roger Hull 275PLANT VIRUS GENE VECTORS FOR TRANSIENT EXPRESSION OF FOREIGN PROTEINS IN PLANTS, Herman B. Scholthof, Karen-Beth G. Scholthof, Andrew O. Jackson 299ROOT SYSTEM REGULATION OF WHOLE PLANT GROWTH, R. M. Aiken, A. J. M. Smucker 325OZONE AND PLANT HEALTH, Heinrich Sandermann Jr 347MORPHOGENESIS AND MECHANISMS OF PENETRATION BY PLANT PATHOGENIC FUNGI, K. Mendgen, M. Hahn, H. Deising 367MICROBIAL ELICITORS AND THEIR RECEPTORS IN PLANTS, Michael G. Hahn 387PATHOGEN QUIESCENCE IN POSTHARVEST DISEASES, Dov Prusky 413

GENETICS OF RESISTANCE TO WHEAT LEAF RUST, J. A. Kolmer 435RECOMBINATION AND THE MULTILOCUS STRUCTURE OF FUNGAL POPULATIONS, Michael G. Milgroom 457QTL MAPPING AND QUANTITATIVE DISEASE RESISTANCE IN PLANTS, N. D. Young 479BREEDING DISEASE-RESISTANT WHEATS FOR TROPICAL HIGHLANDS AND LOWLANDS, H.J. Dubin, S. Rajaram 503CHANGING OPTIONS FOR THE CONTROL OF DECIDUOUS FRUIT TREE DISEASES, Turner B. Sutton 527

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RESISTANCE TO PHENYLAMIDE FUNGICIDES: A Case Study with Phytophthora infestans Involving Mating Type and Race Structure, U. Gisi, Y. Cohen 549STATUS OF CACAO WITCHES' BROOM: Biology, Epidemiology, and Management, LH Purdy, RA Schmidt 573

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1. hibino 1996 rice viruses

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