-'-'~MIT CENTRO DE D OCUMENTACION Chapter 14 Whitefly-Transmitted Viruses G. E. Gálvez and M.R. Cárdenas Page General lntroduction ................................................ ...................... 263 Bean Golden Mosaic Virus lntroduction ........ .................. .. ........ .. ..... ......... ......... .................... 265 Symptomatology ...... ................................................................... 266 Physical Properties ... .. ..... ................................. ................... ....... 267 Transmission and Epidemiology .. ...... ...... ... ..... ......... ................. 269 Control by Cultural Practicas ............. ................ .. ... ................... 271 Control by Chemicals ................... ....... ............. .......................... 272 Control by Plant Resistance ............................. ....... ................... 273 Bean Chlorotic Mottle Virus lntroduction ................ ............. .. ......... ........ ................................. 274 Symptomatology ........ ............... ..................... .............. .... ..... ..... . 275 Physical Properties ............ .. ............. ... .... .. ..... .. ........... .... ..... ...... 276 Transmission and Epidemiology ....... ...................................... ... 276 Control .............. ........ ....... ................... ........ ....... .......... ................ 277 Euphorbia Mosaic Virus lntroduction .. ......... ....... ....... ...... ........ ................................ .... ...... 277 Symptomatology .................. ...... ......... .......... ............ ........... ....... 277 Physical Properties ................... ....................... ........ ................... 278 Transmission and Epidemiology ...... .. ........................................ 278 Control ........... ............ ...... .. ....... ................................. ... .... ........... 278 Rhynchosia Mosaic Virus lntroduction ............... .. .. .... ....... ....... .. .. ........................................ 279 261 Chapter 14 Symptomatology ........ ....................... .......................................... 279 Transmission and Epidemiology ..................................... ........... 280 Control ................................. ......... ............................ ................... 280 Other Whitefly-Transmitted Viruses ............ _. ................................ 280 Literatura Citad .............................................................................. 281 262 Chapter 14 Whitefly-Transmitted Viruses General Introduction Whiteflies belong to the order Homoptera, family Aleyrodidae, and are currently reported to transmit 28 different plant viruses ofbeans and other crops (71, 120). Whitefly species reported to be vectors of plant viruses include Bemisia tabaci Gennadius (=B. inconspicua Quaintance), B. lonicerae, B. manihotis Frappa, B. tuberculata Bandar, B. vayassieri Frappa, Aleurotrachelus socialis Bondar, Aleurothrixus jloccosus Mask, Trialeurodes abutilonea Haldeman, T natalensis Corb. and T vaporariorum Westwood (13, 32, 36, 91, 106). Whitefly populations are commonly restricted to tropical zones below 1300m, where they are capable of transmitting viruses to various plant species (13, 32, 36, 61 , 68, 95, 102, 119, 120). Bemisia tabaci is the most common whitefly vector ofbean viruses and is variable in its feeding habits and reproduction rates on different plant species. Flores and Silberschmidt (56) and Russell (107) characterize this variation as biotypes. However, Bird (9, 10, 11, 14) denotes the variation as races, B. tabaci race jatrophae and B. tabaci race sidae. The virus diseases transmitted by whiteflies (B. tabaci) are grouped into two main types by Costa (52) according to their symptomatology. These types are mosaic and leaf curl. A green, or more frequently yellow, mosaic of foliage is the most conspicuous symptom in the mosaic group. Y ellowing may appear along the veins and develop into a yellow net orbe limited by the veins. Curling or crinkling of the foliage m ay occur dueto the ~bnormal or unequal growth of healthy and infected mosaic areas of the leaf. As the foliage matures, the mosaic tends to become less apparent, and for certain diseases, such as cotton common mosaic, the yellow areas may turn reddish llite in the season (28). In the case of Malvaparviflora infected with the disease agent from Abutilon thompsonii, the initial mosaic is followed by witches' broom symptoms (58). The characteristic yellow or gol den color of infected plants is easy to distinguish from hea1thy plants in a field. . 263 Chapter 14 In the case of leaf curl, infected plants do not exhibit clear mosaic symptoms but may show a diffused yellowing of leaves and vein clearing which may be easily overlooked. The characteristic symptom caused by this group is the stunting of infected plants, curling, enation, and vein thickening of foliage. Costa (36) recently included a third group of whitefly-transmitted viruses which produces yellowing symptoms to distinguish from similar symptoms induced by aphid-transmitted viruses or nutritional disorders. Yellowing symptoms induced by whitefly-transl\}itted viruses commonly appear only later during plant development. Symptomatological differences suggest that the first group of viruses occurs in parenchymatous tissue and the second group occurs in phloem vessels (32). However, sorne diseases may induce symptoms of the first group in sorne hosts and symptoms of the second group in other hosts. F or example, the disease agent from infected Rhynchosia mínima induces a bright yellow mosaic symptom on Rhyncosia mínima but induces leaf curl and enation on tobacco (11). Duffus (54) also mentions two major groups of whitefly-transmitted viruses identified as variegation-producing and plant malformation-producing types. Very few whitefly-transmitted diseases have been isolated and provento have a viral etiology. The previously mentioned groups of viral diseases have been based upon arbitrary classifications due to similarities in symptomatology and presumed insect vectors. Bird et al. (20) suggested that these whitefly-transmitted viruses with unknown or incomplete etiology be placed in one group, rugaceous diseases, instead of different groups primarily distinguished only by symptomatology. Much organized and collaborative research is required to characterize these whitefly- transmitted viruses and establish their true relationships. The following viruses of beans and other plant species have been demonstrated to be whitefly-transmitted, many however, only under research conditions. These viruses are grouped in order of their decreasing economic importance: a) bean golden mosaic; b) bean chlorotic mottle, abutilon mosaic, yellow dwarf mosaic, infectious chlorosis of M alvaceae; e) euphorbia mosaic; d) rhynchosia mosaic; e) jatropha mosaic; f) jacquemontia mosaic; g) ipomoea or merremia mosaic; and h) mung bean yellow mosaic. The following sections of this chapter will review the geographical distribution, economic importance, host range, symptomatology, physical properties, transmission, epidemiology and control measures reported for these viruses. 264 Whitefly-Transmitted Viruses Bean Golden Mosaic Virus Introduction Bean golden mosaic virus (BG MV) was first reported in Latín Ame rica in 1961 (31), at which time it was considered to be a minor disease in Sao Paulo, Brazil. lt has since occurred in practically every major bean production area in Brazil, including Minas Gerais, Parana, Bahía, Pernambuco, Ceara, Para, the Amazon, and the Valle del Rio Sao Francisco (33, 44, 121). BGMV has been reported in many other bean production regions of Latín America, such as El Salvador (66, 67, 126, 127), Guatemala, Nicaragua, Costa Rica, Panama (66, 67), Puerto Rico (12, 17, 21), Jamaica, Dominican Republic (1 , 2, 101, 102, 108), Colombia (63), Cuba (23), Belize, Mexico, Honduras and Venezuela (Gálvez, personal observations). Identification and nomenclature of BGMV has been quite diverse and must be standardized between workers in different regions, since BG MV- like symptoms have been called BGMV, bean yellow mottle, bean golden yellow mosaic, bean yellow mosaic and bean double yellow mosaic(l2, 17, 21, 46, 47, 48, 108, 126, 127). Gálvez et al. (64) utilized serology, electron microscopy and density gradient centrifugation to prove that isolates inducing similar disease symptoms in Mexico, Guatemala, El Salvador, Colombia, Cuba, Puerto Rico, Dominican Republic, Brazil and Nigeria aU were bean golden mosaic virus. This relationship between isolates also should be clarified by utilization of the BGMV antisera developed by Goodman (75) from isolates collected in Puerto Rico. Bean golden mosaic virus is an economically important disease, especially in regions of Latín America such as Brazil and parts of Central America and the Caribbean. Brazilian bean production has been reduced / greatly by the virus since 1972, and its seriousness ha~ been attributed to the increasing whitefly populations associated with the expanded production of soybeans in bean growing areas (33, 44, 121). Gámez (66, 67, 70) considers BG MV to be the principal bean di sea se in the Pacific coastal plains of El Salvador, where disease incidence frequently reaches 100%. Various workers (42, 69, 101, 102) report that infection by BGMV reduces the number of pods, number of seeds per pod and seed weight. Reported yield losses consist of 57% in Jamaica ( 1 O 1, 1 02), 48-85% in Brazil ( 42, 90), 40-100% in Guatemala (96), and 52-100% in El Salvador (Cortez .._-/ and Diaz, personal correspondence). Yield losses vary greatly depending upon plant age at the time of infection, varietal differences and possibly viral strains (33, 6 1). 265 Chapter 14 The host"range of BG MV includes Phaseolus vulgaris, P. luna tus, P. acutifolius, P. polystachios, P. longepedunculatus, P. aborigeneus, P. coccineus, Desmodium occuleatum, Macroptilus lathyroides, Terramnus urcinatus, Vigna radiata, V. unguiculata and Calopogonium muconoides (2, 4, 12, 13, 20, 21, 27, 31, 33, 34, 35, 36, 51, 57, 68, 79, 102, 122, 124). Common names frequently used for bean golden mosaic virus in Latín America include mosaico dorado del frijol, moteado amarillo del frijol and mosaico dourado do feijoeiro. Symptomatology Symptoms of BGMV are readily visible in infected bean plants which exhibit a brilliant yelJow or golden color of lea ves (Fig. 1). Symptoms may appear in the primary 1eaves within 14 days after planting if high populations of whiteflies are present in or near the fie1d. Bird et al. (20, 21) observed the presence of small yellow spots, sometimes apparent as star- shaped lesions, near the leaf veins three to four days after exposure to viruliferous whiteflies. The primary systemic symptoms of BG MV infection are apparent as rolling of the lower leaf surface of young lea ves, which 1ater exhibit a range of mosaic symptoms (Fig. 2). These symptoms are predominant near the veins and within the leaf parenchymatous tissue, where an intense and often brilliant yellowing deve1ops. Susceptible cultivars exhibit a marked rugosity and rolling of lea ves, many of which may be completely yellowed or occasionally white to nearly b1eached. Tolerant cu1tivars often present symptoms with less intense leaf mosaics and may exhibit sorne plant recuperation at a later stage of development. Most cu1tivars do not show a reduction of leaf size (33). When the infection occurs during the seedling stage, susceptible plants may become stunted. Pods of infected p1ants may exhibit mosaic spots orbe malformed (Fig. 3). Seeds may be disco1ored, malformed, and reduced in size and weight (24, 66, 67). The symptomatology of BGMV appears to be similar to that reported for lima bean golden mosaic virus in Africa (122) and lima bean yellow mosaic in India; but the 1atter differs in its host range(95, 105). Mung bean yellow mosaic, urd bean yellow mosaic viruses and yellow mosaic of Do/ichos lablab likewise are not able to infect the majority of Phaseolus vulgaris cultivars (104). However, these viruses appear to have a similar symptomato1ogy on their respective hosts as doesBGMV in beans(92, 93, 95, 104, 128). 266 Whitefly-Transmitted Viruses Fig. 1- Symptoms induced by bean golden mosaic virus in beans. Electron microscopy evaluations of infected bean tissue reveal that the principal cellulu symptom is evident as a drama tic change in chloroplast morphology, particularly in the lamellar system (81). Recently Kim et al. (80) reported that the symptoms are limited to the phloem tissue and cells adjacent to the parenchyma tissue. Virus-like particles appear as packed hexagonal crystal arrangements or as loose aggregates in the nuclei of infected cells. Distinct changes in the nucleoli also are evident, since there is a segregation of granular complexes and fibrils which may occupy 75% of the nuclear volume (76). Physical Properties Bean golden mosaic virus has been classified as a viral disease beca use of its characteristic transmission by insects, symptomatology and mode of dissemination in the field (21 , 31 , 68, 85, 101). However, its viral etiology was not completed until its isolation was accomplished in 1975 by Gálvez and Castaño (62). They observed that fixed BGMV has a specific form which consists of icosahedral particles united in pairs (identical dimer particles or geminates). The bonded particles are flattened at their point of F ig. 2- Mosaic symptoms and leaf malfor- Fig. 3- Pod malformation caused by mation induced by BG MV infection. BG MV infection of a susceptible bean cultivar. 267 Chapter 14 union (Fig. 4) and measure 19 x 32 nm, while individual particles have a diameter of 15-20 nm. Matyis et al. (87) reported individual particles measured 12-13 nm in diameter. A similar particle morphology was found for the viruses causing tomato golden mosaic, euphorbia mosaic (86, 87) as well as BGMV of beans in Brazil, Colombia, El Salvador, Dominican Republic, Guatemala, Mexico, and BG MV of P. luna tus from Nigeria (64). Goodman et al. (77) could not determine whether these geminate particles actually were the infectious entities or artifacts of fixation. However, Gálvez and co-worlcers (24, 62) could observe particles in unflxed preparations, and they gave the highest infectivity. When the BGMV particles were disassociated with EDTA at high molarity(O. IM), infectivity was almost completely lost. BGMV particles have a therrnal inactivation point of 50°C (18, 19) to 55°C (62}, a final dilution end-point of 10-1 ( 62) to 10-2 ( 18, 19), and an in vitro longevity of 48 hours at room temperature (62). Goodman and co- workers (76, 77) deterrnined that the particles have a sedimentation coefflcient value of 69 S, a molecular weight of 2.6 x 1()6 daltons, a 260 nm absorbance value of7.7 anda 260{280 absorbance ratio of 1.4. The genome of BGMV contains DNA which has a sedimentation coefficient of 16 S, a molecular weight of O. 75 x 1()6 daltons, and compases 29% of the particle (24, 25, 72, 73, 76). Two protein components, of molecular weight 3.8 x 1 ()4 and 5.5 x 1()4 daltons, were isolated by Cárdenas and Gálvez (24, 25). The DNA is single stranded and resistant to exonucleases (24, 74). It has a buoyant density of l. 717 g/ mi in cesium chloride and is resolved into two components during polyacrylamide gel electrophoresis in 8 M urea (74, 77). . ~- . =~ '· . ~ • Fig. 4- Geminate particles of bean golden mosaic virus (160,000 X). 268 Whitefly-Transmitted Viruses Francki and Bock (60) have included BGMV in a newvirusgroup called the Geminivirus, based upon its particle characterization, physical- chemical properties and single-stranded DN A. Transmission and Epidemiology BG MV can be transmitted naturally by whiteflies and artificially by mechanical inoculation. Other whitefly-transmitted plant viruses such as euphórbia mosaic, abutilon mosaic and sweet potato virus 8 also ha ve been transmitted mechanically (32, 36). However, Meiners et al. (88) were the first workers to mechanically transmit BGMV to beans. Successful inoculation required a high temperature of 30°C, and a 30% transmission rate was obtained at 24° - 28°C. No transmission occurred below 21 °C. Bird and co-workers (16, 19) originally obtained onJy a 4% transmission but have since improved this efficiency. Gálvez and Castaño (62) obtained nearly 100% transmission under glasshouse conditions at 25°C with BGMV inocuJum extracted from plants infected 21 days earlier in a 0.1 M phosphate buffer at pH 7.5 and 1% 2-mercaptoethanol. Transmission was significantly reduced or zero if inoculum was extracted from plants infected after 21 days. Bird et al. ( 19) utilized a similar buffer at pH 7.0 to obtain 100% transmission by inoculation with an airbrush at 80 lb/ in2. Matyis et al. (87) were notable to transmit BGMV isolates mechanically in Brazil, which may reflect differences in methodology or strains. Sorne strains of BG MV may be transmissible only by the whitefly vector (36, 41, 76). BGMV has not been shown to be transmissible in seed from infected bean plants. Pierre (102) tested seed from 300 infected bean plants, and Costa (31 , 33, 34, 36) tested seed from 350 infected lima bean plants. N one of these seeds was found to be infected by BGMV. The principal mode of BGMV transmission, especially under field conditions, occurs from the whitefly vector, Bemisia tabaci. Whiteflies are able to extract plant sap, but the principal threat to crop productivity is their ability to transmit plant viruses. Costa (32) stated that the whitefly is able to transmit viruses to more than 16 plant species, including cultivated and non-<:ultivated plants. Nene (94) has studied the biology of whiteflies in relation to legumes such as Phaseolus aureus, Vigna mungo and Glycine max. The insect can produce 15 generations a year, during which time populations may be restricted toa single crop species or migra te to a variety of plant species. A 269 Chapter 14 whitefly may la y 38-106 eggs(Fig. 5) during its life cycle, which requires 13- 20 days d uring March to Octo ber or 24-72 days d uring N ovember to M arch in India. Populations of whiteflies are reduced as the mung bean crop matures. These populations then may migrate to other plants such as crucifers, lentils and peas. The life cycle on cotton in India ( 107) varies from 14-107 days, is shortest during April to September (14-21 days), and is longer during November to February (69-72 days). The maximum ovipos,tion occurred at tem- peratures greater than 26.5°C, and no oviposition occurred at temperatures below 24°C . Adults of B. tabaci are able to transmit BGMV in a circulative manner. There is no evidence of transovarial transmission or virus multiplication within the whitefly (32, 36, 95). Costa (32) states that .whitefly-transmitted viruses are not acquired as rapidly as aphid-transmitted viruses. Inoculation efficiency increases more because of longer acquisition periods than because of differences in virus infectivity. Whitefly-transmitted viruses have a defined but shorter incubation period, and particles are retained for more than 20 days in the insect vector. Whitefly adults can acquire and transmit BGMV within 5 minutes (7, 21 , 68), and the inoculation efficiency is increased as population size is increased per infected plant (7, 13, 32, 36, 68, 120). Gámez (68)found an average acquisition and incubation period of three hours each. The retention period varíes according to the acquisition period but may reach 21 days or the entire life ofthe whitefly (7, 20, 32, 36, 68, 120). The insects occasionally have been observed to lose their capacity for transmission (68). lmmature forros (Fig. 6) are able to acquire mung bean yellow mosaic virus which persists during pupation and can be transmitted during the Fig. 5- Eggs and immature forms of Fig. 6- lmmature forms of Bemisia tabaci. Bemisia tabaci on the lower leaf surface. 270 Fig. 7- The adu\t whitefly (Bemis ia tabaci) vector of BGMV. Whitefly-Transmitted Viruses adult stage. At least 50% transmission has occurred from adults (Fig. 7) obtained from irnmature fonns which had previously fed on infected plants (95, 105). Costa (35} reported that female whiteflies were more efficient than males as vectors ofBGMV to Phaseolus vulgaris, P. acutifolius and P. po/ystachios. However, males were more efficient vectors on P. lunatus and P. longepedunculatus. BGMV is not seed-transmitted and, therefore, probably exists in many regions in plant reservoirs such as lima beans and other susceptible legumes including voluntary and cultivated beans, and weeds (34, 36, S l , 52, 61, 68, 1 02). Pierre ( 1 02) considers that lima beans and Macroptilium lathyroides are natural hosts for BGMV in Jamaica, in addition to poinsettias (Euphorbia pulcherrima). Increased production of soybeans has increased whitefly populations and BG MV incidence great\y in beans planted in Parana and Sao Paulo, Brazil (33, 44, 121). Tobacco, tomato and cotton plantings in El Salvador and Guatemala are responsible for the high whitefly populations in those countries (5, 6, 27, 52, 61, 78). Bean golden mosaic virus is more prevalent in lower to intermediate elevations ( 13, 33}, nonnally below 2000 m where whitefly populations, temperatures and inoculum sources are greater. BGMV incidence is less during November to March when temperatures and insect vector populations are lower in Jamaica, Cuba and the Dominican Republic. BG M V is more common and severe in Brazil at elevations between 400-800 m and near the end of the summer or dry period (January to February) when whiteflies migrate from other maturing crops, such as soybeans, to the young bean plantings. Whitefly populations decline rapidly during cooler periods of the year, when temperatures are unfavorable to the whitefly and when fewer susceptible crops exist (31 , 33). Control by Cultural Practices The incidence of BG MV in a bean production region can be reduced by eliminating altemative plant reservoirs of inoculum such as volunteer plants of Phaseolus vulgaris, P. lunatus, P. longepedunculatus, Calopogonium sp. and other plant species. Crop rotation and distribution within a production region also are important. BGMV incidence is 271 Chapter 14 increased greatly by planting beans near fields of soybeans which, although not susceptible to BGMV, are favorable for whitefly populations which may encounter and transrnit BG MV from infected plants, such as Sida spp. and other hosts, to developing bean crops (33, 102). BGMV infection of beans can therefore be reduced by not planting beans near fields of other crops such as soybeans, tomatoes, tobacco and cotton, which favor the build-up of whitefly populations. Date of planting should be varied, if possible, so that young bean plants develop during periods of lower temperature and higher moisture which are less favorable to the whitefly and its ability to transmit BGMV (5, 6, 23, 31' 32, 33, 36, 44, 70, 78, 1 02). N o economical and practical biological control measures are currently available (95, 109). Plant mulches have been shown to reduce whitefly populations (8), possibly due to altered air temperature near the plants. Control by Chemicals The whitefly vector can be controlled by applying insecticides to economically reduce the population size and incidence of BGMV tranmission to susceptible cultivars. Various insecticides are effective against whiteflies (Bemisia tabaci and Trialeurodes vaporariorum). These include Tamaron 600E (l lt / ha), Nuvacron 60 (0.5 lt/ ha), Folimat 1000 (0.5 lt / ha), Bux 360 and Thiodan 35 or End·osulfan (1.5 lt fha) (50). Populations of whiteflies were reduced effectively in El Salvador by applying Tamaron 600 ( 1 lt / ha) every seven days during the first 30 days after plant emergence (53, 82, 83). Alonso (6) reported that Nutasystox R- 25 (1 lt / ha), followed by Nuvacron 50 (1.5 lt / ha) and Folimat 80 (0.33 ltf ha), effectively controlled whiteflies when applied 15 and 30 days after planting. Systemic insecticides, such as Furadan and Thimet, effectively control whitefly populations when applied at planting (6). Substantial yield increases were obtained in the Dominican Republic by applying Carbofuran (Furadan 5G) (2.5 g / m row) at planting followed by 0.15% Monocrotophos (Azodrin 60E) applied at six, 15 and 30 days after plant emergence (3, 89, 99, 100). Nene(94) obtained effective control ofwhiteflies in India with a mixture of (a) 0.1% Thiodan, 0.1% Metasystox and 2% mineral oil, anda mixture of (b) 0.1% Malathion, 0.1% Metasystox and 2% mineral oil. He observed that the mineral oii acted as an ovacide. Chemical control of insect vectors can be effective and economical in areas with moderate to low disease pressure and whitefly populations. However, its effectiveness can be reduced in regions where high numbers of 272 Whitefly-Transmitted Viruses viruliferous vectors migrate continuously from other infected plant species. Therefore, chemical control may have to be combined with other control measures, such as plant resistance, to achieve a higher leve! of protection. Control by Plant Resistance Plant resistance can provide an economical method of disease control. W orkers ha ve evaluated more than 10,000 accessions of Phaseolus vu/garis, and sorne accessions of P. luna tus. P. acutifolius, and P. coccineus under field and laboratory conditions, but they have not found any source of high resistance or immunity to BG MV (24, 26, 27 , 31, 33, 43, 61, 66, 67, ·. 68, 102, 124). However, sorne accessions have exhibited a low to moderate level of resistance or tolerance, including Porrillo 1 and 70, Turria1ba 1, ICA-Pijao, ICA-Tuí, Venezuela 36 and 40, Puebla 441 , Guatemala 388 and 417, and CIAT G-651,-716, -729,-738, -843,-951, -1018, -1069, -1080, -1157, and -1257. Various P. coccineus accessions from the ICTA germplasm bank are resistant in Guatemala. They include Guat. -1278, -1279, -1288, -1291 , -1296, -1299, M7689A and M7719 (24, 26, 27, 79, 124, 125). Pompeu and Kranz (1 03) observed field tolerance in Aete-1 / 37, Aete- 1/ 38, Aete-1 / 40 (Bico de Ouro types), Rosinha GZ/ 69, Carioca 99 and Preto 143/ 106. Rio Tabagi and Goianio Precoce are tolerant in Capinopolis, Brazil (Rava, personal communication). Tulmann-Netoet al. (116, 117, 118) obtained a tolerant mutant, TDM-1 , by treating seed of Carioca with 0.48% ethyl methanol sulfonate for six hours at 20°C. TDM- 1 has a leve! of to1erance similar to that of Turrialba 1, but it is not as agronomically acceptable. The tolerance of Turrialba 1, Porrillo 1, ICA-Tuí and ICA-Pijao has been confirmed in Guatemala, El Salvador, the Dominican Republic, Brazil and N igeria under high disease pressure in bean nurseries inter- planted between tomatoes, tobacco, cotton, and soybeans to favor high whitefly populations (Fig. 8). Glasshouse inoculations and subsequent Fig. 8- Bean golden mo:>a•g.: virus screening nursery the Dominican ~epublic. 273 Chapter 14 laboratory analyses revealed that these tolerant materials contained lower virus concentrations than highly susceptible accessions (24, 26, 27). These tolerant materials have been utilized in breeding programs, and initial progenies appear promising (65, 129). Sorne progenies are highly tolerant to BGMV and produce 1,500 kg/ ha under high disease pressure, as compared to yields of 1,000 (ICA-Pijao) and 650 (Turria1ba l) kg/ ha for the progenitors. These progenies can produce 3,000 kgfha in conditions where the virus is not a limiting factor to production. Bean golden mosaic virus and its whitefly vector are able to survive on and infect various p1ant species, including beans. Integrated control measures can effective1y reduce the incidence and severity of BG MV. These measures should consist of reducing vector populations by chemicals, eliminating altemative hosts, and using different p1anting dates combined with the deve1opment of agronomicaUy acceptable cultivars with improved levels of to1erance or resistance. Bean Chlorotic Mottle Virus Introduction Bean chlorotic mottle virus (BC1MV), abuti1on mosaic virus (AbMV), yellow dwarf mosaic virus and infectious ch1orosis of Malvaceae have a similar symptomato1ogy and are considered as a group in this section. Additional research is required to fully characterize these viruses to determine whether or not they are identical. These viruses reportedly are widespread throughout Latín America, wherever the whitefly vector exists (4, JO, 12, 13, 14, 15, 16, 36, 38, 45, 78). They have been observed in Colombia, Mexico, Guatemala, El Salvador, Costa Rica, Cuba, Dominican Republic, Jamaica, Trinidad, Tobago, Venezuela, Ecuador, Peru, Bolivia and the United States. Often they are present in regions where bean golden mosaic virus and Rhynchosia mosaic virus exist. Their symptoms frequently are confused with those of BClMV and AbMV (27, 29, 31, 32, 36, 61, 97, 111, 113, 123). Common names frequently used for bean chJorotic mottle virus and abutilon mosaic virus in Latín America include moteado clorótico del fríjol, enanismo amarillo, enanismo del fríjol, anao amarelo, clorosis infecciosa de las Malvaceas, and mosaico de Abutilon. BClMV can cause 100% infection in susceptible cultivars but seldom is economically importan t. Its incidence normally is onJy 2-5% in Brazil (31 ). However, Costa (33) reported that BClMV caused 100% yield loss in each of five cultivars that he studied. 274 ·. Fig. 9- Plant stunting and witches' broom produced by the bean chlorotic mollle virus. Whitefly-Transmitted Viruses This group of viruses has a wide host range which includes Phaseolus vulgaris, P. lunatus. Abutilon hirtum Sweet, Althere rosea (L.) Cav., Bastardfa viscosa (L.) H.B.K., Corchorus aestruans L., Gossypium barbadense L., G. hirsutum L., G. esculentum Mili. , Hibiscus brasi/ensis L., H. esculentus L., Malva parviflora L., Malva silvestris L. , Malvaviscus sp., Sida acuminata D .C., S. aggregata Presl., S. bradei Ulbricht, S. carpinifolia L., S. cardifolia L., S. glabra Mili., S. glomerata Cav., S. humilis Cav., S. micrantha St. Hit., S. procumbens Sw., S. rhombifolia L., S. urens L., Datura stramonium L. , Nicandra physaloides Gaertn., Nicotiana glutinosa L., N. tabacum L., Solanum tuberosum L., Arachis hypogea L., Canavalia ensiformis D.C., Cyamopsis tetragonalobus (L.) Taub., Glycine max(L.) Merr. , Lens culinaria Medik., L esculenta Moench. , Lupinus a/bus L. and Pisum sativum L. (JO, 12, 13, 14, 15, 20, 29, 30, 31, 39, 40, 45, 49, 55, 59, 61, 78, 81, 98, 110, 111, 112). Symptomatology BCIMV and AbMV infection can cause asevere dwarfing of susceptible plants, accompanied by a high proliferation of buds and a bunchy or rosette type of plant development. If infection occurs in young plants, a witches' broom is produced and leaves often exhibit chlorotic mottling (Fig. 9). Chlorotic spots or mottled areas may be produced on leaves of tolerant cultivars or older susceptible plants (Fig. 10). These spots may be accompanied by a rugosing of leaves (Fig. 11). Severely affected plants Fig. 10- hlorotJc m o lile symptoms Fig. 1 1- Leaf rugosing suspected to be induced by produced on leaves infected by BCIMV. BCIMV. 275 Chapter 14 Fig. 12- Chlorotic mottling induced by AbMV infection of Pavonia sidaefo /ia. Fig. 13- lnfectious chlorosis of Malvaceae symptoms induced in an infected Malva sp. plan t. produce few or no pods. Figure 12 illustrates AbMV symptoms produced in an infected Pavonia sp. plant, and Figure 13 illustrates symptoms of infectious ch1orosis of Ma1vaceae in an infected Malva sp. plant. Physical Properties S un (115) observed ultrathin cytoplasmic sections of Abutilon stn'atum var. thompsonii infected with AbMV and found spherical particles 80 nm in diameter. These particles consisted of an inner core 16 nm in diameter surrounded by an outer shell. Kitajima and Costa (8 I) observed isometric particles 20-25 nm in diameter in infected tissue of Sida micrantha. Additional studies are needed to compare these observations with BCIMV isolated from other infected hosts including beans. Costa and Carvalho (39, 40) determined that AbMV had a thermal inactivation point of 55° - 60°C, a final di1ution end-point of 5-6, and retained its infectivity for 48-72 hours in vitro in water or sodium sulfide buffer. Transmission and Epidemiology Mechanical transmission of AbMV has been very difficult but has been accomplished by Costa and Carvalho (39, 40) from Malva parviflora and Sida micrantha to soybeans. The virus can be propagated in these species as well as in Sida carpinifolia. Bird et al. (20) was unable to transmit AbMV mechanically and had difficulties with its natural vector, Bemisia tabaci race sidae. Strain differences may exist within the virus and whiteflies. Whiteflies have been demonstrated to transmit BClMV and AbMV to beans ( 1 O, 20, 29, 30, 31 , 33, 36, 38, 56, 97, 113, 114). Bird et al. (20) showed that whiteflies could acquire the virus during a 15-20 minute feeding and retain their ability to transmit AbMV for seven days. Costa (33) was able to transmit AbMV easily from Sida sp. to beans but had difficulty transferring it from beans to beans via the whitefly. 276 Whítefly-Transmítted Víruses Studies have not found BC!MV or AbMV to be seed transmitted (20). These viruses appear to ha ve a wide host range, including many tropical weed species, which serve as inoculum sources from which whitefly populations acquire the virus and transmit it to beans. Epidemics of AbMV and BClMV also may occur in beans when large plantings of other susceptible crops such as soybeans and cotton, are planted nearby (27, 31, 61, 123). Control ·, Very little research exists concerning control measures. However, Costa (31, 36) did not encounter any resistance within Phaseolus vulgaris in Brazil. Resistance was found in other species of Phaseo/us, such as P. angularis, P. aureus, P. calcara tus and P. trinervius (31 ). The following P. vulgaris accessions were observed to be resistant to BClMV during a natural epidemic at CIA T: ICA - Tuí, Trujillo 7, Honduras 4, P .l. 307824 and P.l. 310739. Additional research is required to verify the resistance of these materials and the practicality of incorporating their resistance into agronomically desirable backgrounds. Euphorbia Mosaic Virus Introduction Euphorbia mosaic virus (EMV) was isolated in 1950 from Euphorbia prunifolia Jacq. (37) and has since been observed in many species of Euphorbia. The virus has been detected in beans in Brazil but does not appear to be economically important. Common names frequently used for EMV in Latín America include mosaico de las Euforbiaceas and encarquilhamente da folha. The host range of EMV includes Euphorbia prunifolia, Datura stramonium, Lycopersicon esculentum, Nicandra physaloides, Nicotiana glutinosa, Canavalia ensiformis, Glycine max, Lens esculenta and Phaseolus vulgaris ( 18, 20, 22, 3 1, 33, 36, 40). Symptomatology EMV or bean crumpling generally produces only local necrotic leaf lesions at the feeding sites of viruliferous whiteflies. Occasionally EMV may induce a systemic infection characterized by twisting or crumpling of leaves due to the unequal growth of green tissue surrounding the initial necrotic lesions. A bnormal development of auxillary buds al so may occur, and plants are commonly stunted. 277 Chapter 14 Physical Properties M a tyis et al. (86, 87) purified EMV partially and reported that it consists of identically-paired particles 25 nm in diameter and individual isometric particles which measure 12 - 13 nm in diameter. They determined that EMV belongs to the Geminivirus group. Costa and Carvalho (39, 40) reported that EMV in sap has a thermal inactivation point of 55° - 60°C and retains its infectivity in vitro for more than 48 hours. Bird et al. (18) also report that EMV has a thermal inactivation point of 55° - 60°C but retains its infectivity in vitro less than 24 hours and has a dilution end point of 10-J. lnfectivity can be maintained : in tissue dried in calcium chloride at 4°C for 12 weeks. Transmission and Epidemiology Euphorbia mosaic virus can be transmitted mechanically from Euphorbia sp. (Fig. 14) to Datura sp. at a rate of 31% and easily between Datura sp. (18, 22, 39, 40). Transrnission from soybeans to soybeans is difficult. EMV is not seed-transmitted (20, 33). Bemisia tabaci supply the natural mode of transmission, can acquire the virus during a 1 O-minute feeding period, but require a 20-rninute period for transmission, and can retain their infectivity for 20 days (20, 31 , 36, 37). Euphorbia mosaic virus seldom is observed in bean fields unless there is a high incidence of whiteflies and infected Euphorbia spp. near or within the field. Control Very Jittle research has been conducted on control measures for EMV, which is even less infectious to beans than BCJMV or AbMV (31 , 33, 36). However, plant resistance has been identified in accessions of Phaseolus 278 Fig. 14- Leaf wrinkling and chlorosis of an Euphorbia sp. plant infected with Euphorbia mosaic virus. Whitefly-Transmitted Viruses angularis. P. aureus. P. calcara tus and P. trinervius. Additional research is required to determine if resistance exists within P. vulgaris and is practica! as a control measure. Rhynchosia Mosaic Virus Introduction Rhynchosia mosaic virus (RMV) was isolated in Puerto Rico and produces symptoms similar to those reported for infected Rhynchosia mínima in other tropical countries (ll, 12, 13, 14, 15, 20, 84). Symptoms of RMV are similar to those caused by BCIMV and AbMV. Research is required to determine the relationship between these viruses. Rhynchosia mosaic virus is transmitted by whiteflies but is not reported to cause economic problems. The common name frequently used for Rhynchosia mosaic virus in Latin America is mosaico de la Rhynchosia. The virus has a host range which includes Salvia splendeus Sellow, Cajanus indicus Spreng, Canavalia ensifomis (L.) D.C., C. marítima (Aubl.) Thou., Crotalaria juncea L., Glycine max (L.) Merrill, Macroptilium lathyroides (L.) Urban, Pachyrrhizus erosus (L.) Urban, Phaseolus aborigeneus Burk., P. acutifolius A. Gray. P. l. Wright, P. acutifolius A. Gray latifolius, P. coccineus L., P. lunatus L. , P. trichocarpus C. Wright, P. vulgaris L., Rhynchosia mínima DC, R. reticulata DC, Vigna aconitifolia (Jacq.) Marechal, V. angularis (Willd.) Ohwi and Ohashi, Abelmoschus esculentus (L.) M oendi, Gossypium hirsutum L., Malachra capitata L. , Oxalis berrelieri L., Nicotiana acuminata Hook, N. afata Link and Otto, N. bonariensis Lehmann, N. glutinosa L., N. nightiana Goodspeed, N. marítima Wheeler, N. paniculata L.and N. tabacum L. ( 11 , 20). Symptomatology Rhynchosia mosaic virus infection of beans causes symptoms such as leaf malformation, yellowing (Fig. 15), witches' broom and plant stunting . Fig. 15- Bean leaves infected with Rhynchosia mosaic virus. 279 ........-:: Chapter 14 When infection occurs in young plants, symptoms consist of a proliferation of flowers and branches and little if any seed production ( 14). The virus has not yet been purified to study its physical properties. Transmission and Epidemiology Mechanical transmission ( 18%) has been demonstrated by using buffers and the tobacco cultivar, Virginia 12, as source of inoculum (12, 20). Rhynchosia mosaic virus has not been found to be seed-transmitted (20). The virus is easily transmitted by Bemisia tabaci (11, 20). Transmission can be achieved in less than 24 hours and the insect retains its infectivity for seven days. Apparently, the virus survives in infected weeds such as Rhynchosia minima which is widespread throughout the tropics. Control Very little research has been conducted into control meas u res for RM V. Glasshouse investigations in Puerto Rico (20), revealed that the bean cultivars La Vega (R 19) and Santa Ana (selection from Masa ya, Nicaragua) were tolerant to the virus and hada good leve! of resistance in the field . Other Whitefly-Transmitted Viruses Bird (9,20) reports that three viruses were capable of infecting beans under controlled conditions in Puerto Rico. They were Jatropha mosaic virus, isolated from Jatropha gossypifo/ia (L.) Pohl and transmitted by Be misia tabaci race (biotype) jatropha; Merremia mosaic virus, isolated from Merremia quinquefolio Hall and transmitted by Bemisia tabaci race (biotype) sidae; and Jacquemontia mosaic virus, isolated from Jac- quemontia tamnifolia Griseb and transmitted by Bemisia tabaci race (biotype) sidae. This chapter has reviewed briefly sorne of the whitefly-transmitted viruses which are reported to infect beans under natural and artificial conditions. Much confusion exists between investigators as to virus identification and relationships (20, 33, 36, 41, 61 , 76, 86). Additional research is required to elucidate this complex group ofviruses and to study the variability which may exist within these viruses and their whitefly vectors. 280 Whitefly-Transmitted Viruses Literature Cited 1. Abreu-R., A. 1978. Identificación del mosaico dorado de la habichuela (Phaseolus vulgaris L.) en República Dominicana. Investigación 6: 21-24. 2. Abreu-R., A. and G. E. Gálvez. 1979. Identificación del mosaico dorado del frijol (Phaseolus vulgaris L.) en República Dominicana. In, Memoria Programa Cooperativo Centroamericano para el Mejoramiento de Cultivos Alimenticios (P.C.C.M.C.A.), XXV Reunión Anual, Tegucigal- pa, Honduras, March 19-23, Vol. 3: LlS/ 1-2. 3. Abreu-R. , A., C.E. Peña and G. E. Gálvez. 1979. Control del virus del mosaico dorado del frijol (Phaseolus vu/garis L.) por resistencia varietal y por control químico del insecto vector, Bemisia tabaci Genn. In. XXV Reunión Anual del P.C.C.M.C.A., Tegucigalpa, Honduras, March 19-23, Vol. 3: L 14/ 1-3. 4. Agudelo-S., F. 1978. Revisión de trabajos hechos en Latinoamérica sobre virus de la habichuela (Phaseolus vulgaris L.) y su relación con el mosaico dorado de este cultivo en la República Dominicana. Investigación 6: 43-46. 5. Alonzo-P., F. 1975. Estudios en PhaseolusvulgarisL.sobrecontroldemosca blanca Bemisia tabaci Genn. en la zona sur-oriente de Guatemala. Paper presented at Workshop on Bean Production, CIAT, Cali, Colombia, Dec. 1-3, 18 p. 6. Alonzo-P., F. 1976. Uso de insecticidas granulados en frijol para el combate de Empoasca sp. y Bemisia rabaci (Genn.) en el Sur-oriente de Guatemala. In, XXII Reunión Anual del P.C.C.M.C.A. , San José, Costa Rica. 7. Arevalo-R., C. E. and A. J . Díaz-Ch. 1966. Determinación de los periodos mínimos requeridos por Bemisia rabaci Genn. en la adquisición y transmisión del virus del mosaico dorado del frijol. In, XII Reunión Anual del P.C.C.M.C.A., San José, Costa Rica. 8. Avidov, Z. 1957. Bionomics of the tobacco whitefly (Bemisia tabaci Genn.) in Israel. Ktavim (Rec. Agr. Res. Sta., Rehovot), 7: 25-41. 9. Bird, J . 1957. A whitefly-transmitted mosaic of Jatropha gossypifolia. Agr. Exp. Sta., Univ. Puerto Rico, Tech. Paper 22: 1-35. 10. Bird, J . 1958. Infectious chlorosis of Sida carpinifolia in Puerto Rico. Agr. Exp. Sta. , Univ. Puerto Rico, Tech. Paper 26: 1-23. 11. Bird, J . 1962. A whitefly-transmitted mosaic of Rhynchosia minima and its relation to tobacco leaf curl and other virus diseases of plants in Puerto Rico. Phytopathology 52: 286 (Abstr.). 12. Bird, J . and J. H. López-Rosa . 1973. New whitefly and aphid-bome viruses of bean (Phaseolus vulgaris) in Puerto Rico. In , Grain Legume Improvement Workshop, Oct. 29- Nov. 2, liTA, Ibadan, Nigeria, 6 p. 281 Chapter 14 13. Bird. J. and K. Maramorosch. 1978. Viruses and virus di sea ses associated with whiteflies. Adv. in Virus Research 22:55-110. 14. Bird. J. and J . Sánchez. 1971. Whitefly-transmitted viruses in Puerto Rico. J. Agr. Univ. Puerto Rico 55: 461-466. 15. Bird. J .. J. Sánchez and J.H. López-Rosa. 1970. Whitefly-transmitted viruses in Puerto Rico. Phytopathology 60: 1539 (Abstr.). 16. Bird. J., J . Sánchez and R. Rodríguez. 1974. Viruses affecting soybeans in Puerto Rico. Proc. of the Workshop on Soybeans for Tropical and Sub- tropical Conditions. Univ. Puerto Rico. Mayaguez Campus. Intsoy Pub. Series 2. pp. 109-111. 17. Bird. J .. J. Sánchez and N.G. Vakili. 1973. Golden yellow mosaic ofbeans (Phaseolus vu/garis) in Puerto Rico. Phytopathology 63: 1435. 18. Bird. J., A. Cortes-Monllor, J . Sánchez and R. L. Rodríguez. 1977. Propiedades de dos virus transmitidos por la mosca blanca &misia tabaci Genn. en Puerto Rico. Fitopat. 12: 31-32. 19. Bird. J., R. L. Rodríguez. A. Cortés-Monllor and J. Sánchez. 1977. Transmisión del mosaico dorado de la habichuela ( Phaseolus vulgaris) en Puerto Rico por medios mecánicos. Fitopat. 12: 28-30. 20. Bird. J .. J . Sánchez, R. L. Rodríguez and F . J . Julia. 1975. Rugaceous (whitefly-transmitted) viruses in Puerto Rico. pp. 3-25. In, Tropical Diseases of Legumes. J. Bird and K. Maramorosch, eds. Academic Press, New York. 21. Bird. J ., J. E. Pérez, R. Alconero, N. G. Vakili and P . L. Meléndez. 1972. A whitefly-transmitted golden-yellow mosaic virus of Phaseolus lunatus in Puerto Rico. J. Agr. Univ. Puerto Rico 56: 64-74. 22. Bird. J .. M. Kimura. A . Cortés-Monllor, R. L. Rodríguez, J. Sánchez and K. Maramorosch. 1975. Mosaico de Euphorbia prunifolia Jacq. en Puerto Rico: Transmisión. Hospederas y Etiología. In. Memoria XX I Reunión Anual del P.C.C.M.C.A. , Vol. 1: 233-234. 23. Blanco Sánchez. N. and l. Bencomo. 1978. Afluencia de la mosca blanca (&misia tabaci), vector del virus del mosaico dorado. en plantaciones de fríjol. Ciencias de la Agr. 2: 39-46. 24. Cárdenas-A .. M. R. 1977. Estudios sobre el virus del mosaico do rado del frijol (BGMV). Mg. Se. Tesis., Programa Estudios Graduados. Univ. Nal. !CA, Bogotá. Colombia. 80 p . 25. Cárdenas-A., M. and G. E. Gálvez-E. 1977. Extracción e infectividad del ácido dexoxiribonucléico (DNA) de los mosaicos dorados del frijol (BGMV) América Latina y del frijol lima (LBGMV) de A frica. Proc. Amer. Phytopath. S oc. 4: 175 (Abstr.). 26. Cárdenas-A., M. and G. E. Gálvez-E. 1977. Concentración del mosaico dorado del fríjol (BGMV) en variedades susceptibles y tolerantes de frijol ( Phaseolus vulgaris L.) y su relación con diferentes órganos de la planta. Proc. Amer. Phytopath. Soc. 4:175 (Abstr.). 282 Whitefly-Transmitted Viruses 27. CIAT. 1973-1978. Annual Reports ofthe Bean Production Program. Centro lnternational de Agricultura Tropical, Cali, Colombia. 28. Costa, A.S. 1937. Nota sobre o mosaico dourado do algodoeiro. Rev. Agr. Piracicaba 12: 453-4 70. 29. Costa , A. S. 1954. ldentidade entre o mosaico comun do algodoeiro e a clorose infecciosa das malváceas. Bragantia 13: 23-27. 30. Costa, A.S. 1955. 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