EPPO quarantine pest Prepared by CABI and EPPO for the EU

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Data Sheets on Quarantine Pests

Bean golden mosaic bigeminivirus

IDENTITY
Name: Bean golden mosaic bigeminivirus
Taxonomic position: Viruses: Geminiviridae: Bigeminivirus
Common names: BGMV (acronym)
Bean golden mosaic, bean golden yellow mosaic (English)
Mosaico dorado (Spanish)
Notes on taxonomy and nomenclature: Brown (1990) reviewed the geminiviruses of
legumes in Latin America and the Caribbean, covering isolates which have been named as
BGMV and others which have been given different names, especially bean calico mosaic
(Brown et al., 1990) and bean dwarf mosaic (Morales et al., 1990; Morales, 1991). She
concluded that the relationships between all these viruses needed to be further studied.
Swanson et al. (1992) found BGMV to be serologically related to bean calico mosaic,
cotton leaf crumple, serrano golden mosaic and squash leaf curl geminiviruses; a probe for
its DNA-A detected nearly all American geminiviruses, while its DNA-B gave a weak
positive reaction with a probe for bean calico mosaic geminivirus. BGMV also has some
serological relationship with the Old World mungbean yellow mosaic geminivirus
(Shimizu et al., 1987), but in general the Old World legume geminiviruses are quite distinct
from BGMV.
EPPO computer code: BNGMXX
EPPO A1 list: No. 204
EU Annex designation: I/A1

HOSTS
The principal cultivated hosts of BGMV are Phaseolus vulgaris and P. lunatus. The
different isolates have been found to infect a range of wild Fabaceae, especially the
common weed Macroptilium lathyroides and also species of Phaseolus, Vigna and
Calopogonium. BGMV is restricted in its host range to Fabaceae, though it has been
suggested that the malvaceous weed Malvastrum coromandelianum may be a host. The
closely related bean calico mosaic geminivirus occurs essentially on P. vulgaris. Symptoms
of golden mosaic (Brown, 1990) have also been seen on: Phaseolus longepedunculatus and
Vigna luteola in Brazil; soyabeans (Glycine max) in Venezuela; P. acutifolius and P.
coccineus in Central America.

GEOGRAPHICAL DISTRIBUTION
Golden mosaic symptoms have been seen on legumes in many countries of tropical
America. In many cases, BGMV has specifically been identified, and these cases are
indicated as unqualified records below. In other cases, a related virus has been identified or
only symptoms have been seen. Since the relationships between BGMV and similar viruses
have not yet been fully worked out, these other records (Brown, 1990) are also mentioned
here.
2 Bean golden mosaic bigeminivirus

EPPO region: Absent.

North America: Mexico (Sonora, bean calico mosaic and cotton leaf crumple; Chiapas,
Sinaloa and Yucatan, symptoms only), USA (Florida).
Central America and Caribbean: Costa Rica, Cuba, Dominican Republic, El Salvador
(symptoms only), Guatemala, Jamaica, Nicaragua (symptoms only), Panama (symptoms
only), Puerto Rico.
South America: Argentina, Brazil (widespread, including Goias, Rio Grande do Sul, São
Paulo), Colombia, Venezuela; widespread in tropical and subtropical America.
EU: Absent.

BIOLOGY
BGMV is transmitted in a persistent manner by Bemisia tabaci. Adults can acquire the
virus in as little as 6 min. BGMV is retained for days or weeks, and through the moult.
It does not multiply in the vector and is not transmitted directly to progeny. Non-vector
transmission is by mechanical inoculation (with the exception of isolates from Argentina
and Brazil), by grafting, but not by contact between plants. The virus is not transmitted by
seed or pollen. The normal source of inoculum is adjacent bean crops, or leguminous
weeds.
After inoculation of primary leaves with BGMV, symptoms appear 5-6 days later on
trifoliate leaves. The virus multiplies and spreads in the phloem and phloem-associated
cells, and finally enters the mesophyll. The titre of BGMV peaks about 10-12 days after
inoculation. Symptom development depends on temperature: symptoms are more
pronounced and appear earlier at 27-30°C than at 21-24°C (when they may take several
weeks to appear) (Haber et al., 1991).
Relationships between BGMV isolates from different American countries are still being
worked out. The original isolate from Colombia (BGMV-CO) has been less fully
documented than the isolate from Puerto Rico (BGMV-PR) (Goodman, 1977; Goodman &
Bird, 1978). The isolate from Venezuela (BGMV-VE) differs in DNA hybridization
analysis from BGMV-PR (Debrot et al., 1986). Nardo & Costa (1986) have differentiated
five isolates of BGMV in Brazil on the basis of severity of infection. An isolate (BGMV-F)
has been described in Florida (USA) (Hiebert et al., 1991). One strain from Goias (Brazil),
BGMV-BZ, differs from Central American and Caribbean isolates, including those from
the Dominican Republic (BGMV-DR) and Guatemala (BGMV-GA), in not being sap-
transmissible and in sequence homology (Gilbertson et al., 1991a,b, 1993). Isolates from
Argentina are also not mechanically transmissible (Haber et al., 1991).

DETECTION AND IDENTIFICATION

Symptoms
Vein yellowing, netting and clearing, extending to bright-yellow interveinal chlorosis.
Leaves emerging after symptoms have first appeared curl down, fail to expand and become
stiff and leathery. Seed set is poor (Haber et al., 1991).
Morphology
Geminate particles, 18-20 nm in diameter and 30 nm in length. BGMV has been much
studied in relation to the characterization of geminiviruses, e.g. first demonstration of a
bipartite genome (Haber et al., 1981). Isolates BGMV-PR and BGMV-BZ have been fully
sequenced (Howarth et al., 1985; Gilbertson et al., 1993).
Bean golden mosaic bigeminivirus 3

Detection and inspection methods

Preparations of BGMV are immunogenic. The virus reacts in standard gel diffusion tests
and is also detectable by ELISA. The recommended indicator plant is Phaseolus vulgaris
cv. Top Crop, which gives conspicuous systemic vein chlorosis and golden mosaic.

MEANS OF MOVEMENT AND DISPERSAL

BGMV moves only in its vector Bemisia tabaci, which can spread it between fields in
infested areas. In international trade, it is very unlikely to be carried by plants of Phaseolus
spp., since these are short-lived vegetable; crops not normally moved. The vegetables as
such would not be likely to carry B. tabaci, and the disease is not seed-transmitted. So the
main risk of movement is in B. tabaci on other host plants (e.g. ornamentals), given the fact
that the vector moves readily from one host to another and that the virus can persist in the
vector for several weeks after acquisition.

PEST SIGNIFICANCE
Economic impact
BGMV, first described in Colombia in 1976 (Galvez & Castanõ, 1976), is reported as the
most devastating disease of beans in Latin America (Galvez & Cardenas, 1980). Losses up
to 75% have been recorded in Brazil (Menten et al., 1980; Almeida et al., 1984; Fazio,
1985). This has been associated with marked increases in the populations of Bemisia tabaci
since the 1970s, BGMV first being recorded there in 1979 (Barreto et al., 1980).
The disease continues to increase in importance in Latin America and the Caribbean,
especially in situations where bean crops are planted alongside sources of the vector, so
that they become infested early and the disease can spread readily. The increasing
abundance of B. tabaci biotype B on many hosts favours this early infestation.
Control
Bean crops should be planted at times, or in places, where they are not exposed to high
populations of B. tabaci. Sources of inoculum (leguminous weeds) should be removed or
controlled. Chemical control of the vector (e.g. with carbofuran + monocrotophos in Brazil;
Farias & Zimmermann, 1988) does reduce disease incidence and increase yields, but such
treatments have not generally proved very practical. Coloured mulches may be used to
reduce whitefly populations. Resistance to BGMV is important in bean breeding, e.g. at
CIAT (Schwartz & Sanders, 1979; Morales & Niessen, 1988), though up till now only
moderate resistance has been found (Haber et al., 1991). The coat protein genes of BGMV
have been successfully genetically engineered into Phaseolus (Russell et al., 1993), but it is
not clear whether they confer resistance.
Phytosanitary risk
BGMV was recently added to the EPPO A1 list but has not been considered a quarantine
pest by any other regional plant protection organization. It clearly presents a considerable
danger to legume crops in the Old World tropics. For the EPPO region, crops of Phaseolus
vulgaris would be at risk throughout the more southern parts. With its preference for P.
vulgaris, it certainly presents a much greater risk to the EPPO region than the similar Old
World geminiviruses (mungbean yellow mosaic, horsegram yellow mosaic), adapted to Old
World Vigna spp. not cultivated in Europe, or than the "non-European B. tabaci-
transmitted" cowpea mild mottle 'carlavirus' (EPPO/CABI, 1996).
4 Bean golden mosaic bigeminivirus

PHYTOSANITARY MEASURES
Host plants of Bemisia tabaci from areas where BGMV occurs should come from a place
of production free from BGMV and B. tabaci (or treated against B. tabaci) during the last
growing season. This applies especially to the ornamental Euphorbia pulcherrima, which is
notorious for carrying B. tabaci inconspicuously.

BIBLIOGRAPHY
Almeida, L.D. de; Pereira, J.C.V.N.A.; Ronzelli, P.; Costa, A.S. (1984) [Evaluation of losses caused
by golden mosaic of bean (Phaseolus vulgaris) under field conditions]. Fitopatologia Brasileira 9,
213-219.
Barreto, B.A.; Silva, T.L. da; Teixeira, R.M. de C. (1980) [Occurrence of the whitefly Bemisia tabaci
on bean (Phaseolus vulgaris) in the state of Rio Grande do Sul]. Agronomia Sulriograndense 16,
363-365.
Brown, J.K. (1990) An update on the whitefly-transmitted geminiviruses in the Americas and the
Caribbean Basin. FAO Plant Protection Bulletin 39, 5-23.
Brown, J.K.; Chapman, M.A.; Nelson, M.R. (1990) Bean calico mosaic, a new disease of common
bean caused by a whitefly-transmitted geminivirus. Plant Disease 74, 81.
Debrot, C.E.; Lastra, R.; Uzcategui, R.C.; Haber, S. (1986) Occurrence of a golden mosaic of
legumes in Venezuela. Plant Disease 70, 981.
EPPO/CABI (1996) Cowpea mild mottle 'carlavirus'. In: Quarantine pests for Europe. 2nd edition
(Ed. by Smith, I.M.; McNamara, D.G.; Scott, P.R.; Holderness, M.). CAB INTERNATIONAL,
Wallingford, UK.
Farias, J.C.; Zimmermann, M.J.O. (1988) [Control of bean golden mosaic by means of varietal
resistance and insecticides]. Fitopatologia Brasileira 13, 32-35.
Fazio, G. de (1985) [Bean golden mosaic in Brazil]. Fitopatologia Brasileira 10, 41-48.
Galvez, G.E.; Castanõ, M. (1976) [Purification of the whitefly-transmitted bean golden mosaic virus].
Turrialba 26, 205-207.
Galvez, G.E.; Cardenas, M.R. (1980) In: Bean production problems (Ed. by Schwartz, H.P.; Galvez,
G.E.). CIAT, Cali, Colombia.
Gilbertson, R.L.; Faria, J.C.; Hanson, S.F.; Morales, F.J.; Ahlquist, P.; Maxwell, D.P.; Russell, D.R.
(1991a) Cloning of the complete DNA genomes of four bean-infecting geminiviruses and
determining their infectivity by electric discharge particle acceleration. Phytopathology 81, 980-
985.
Gilbertson, R.L.; Hidayat, S.H.; Martinez, R.T.; Leong, S.A.; Faria, J.C.; Morales, F.; Maxwell, D.P.
(1991b) Differentiation of bean-infecting geminiviruses by nucleic acid hybridization probes and
aspects of bean golden mosaic in Brazil. Plant Disease 75, 336-342.
Gilbertson, R.L.; Faria, J.C.; Ahlquist, P.; Maxwell, D.P. (1993) Genetic diversity in geminiviruses
causing bean golden mosaic disease: the nucleotide sequence of the infectious cloned DNA
components of a Brazilian isolate of bean golden mosaic geminivirus. Phytopathology 83, 709-
715.
Goodman, R. (1977) Single-stranded DNA genome in a whitefly-transmitted plant virus. Virology 83,
171-179.
Goodman, R.M.; Bird, J. (1978) Bean golden mosaic virus. CMI/AAB Descriptions of Plant Viruses
No. 192. Association of Applied Biologists, Wellesbourne, UK.
Haber, S.; Ikegami, M.; Bajet, N.B.; Goodman, R.M. (1981) Evidence for a divided genome in bean
golden mosaic virus, a geminivirus. Nature, UK 289, 324-326.
Haber, S.; Maxwell, D.P.; Gilbertson, R.L. (1991) Bean golden mosaic. In: Compendium of bean
diseases, pp. 42-43. American Phytopathological Society, St. Paul, USA.
Hiebert, E.; Wisler, G.C.; Purcifull, D.E.; Sanchez, G.; Morales, F.J. (1991) Characterization of a
Florida bean golden mosaic virus (BGMV-F) isolate. Phytopathology 81, 1242-1243.
Howarth, A.J.; Caton, J.; Bossert, M.; Goodman, R.M. (1985) Nucleotide sequence of bean golden
mosaic virus and a model for gene regulation in geminiviruses. Proceedings of the National
Academy of Sciences of the USA 82, 3572-3576.
Bean golden mosaic bigeminivirus 5

Menten, J.O.M.; Tulmann Neto, A.; Ando, A. (1980) [Evaluation of damage caused by the bean
golden mosaic virus (BGMV)]. Turrialba 30, 173-176.
Morales, F.J. (1991) Bean dwarf mosaic. In: Compendium of bean diseases, pp. 41-42. American
Phytopathological Society, St. Paul, USA.
Morales, F.J.; Niessen, A.I. (1988) Comparative responses of selected Phaseolus vulgaris germplasm
inoculated artificially and naturally with bean golden mosaic virus. Plant Disease 72, 1020-1023.
Morales, F.J.; Niessen, A.I.; Ramirez, B.; Castanõ, M. (1990) Isolation and partial characterization of
a geminivirus causing bean dwarf mosaic. Phytopathology 80, 96-101.
Nardo, E.A.B. de; Costa, A.S. (1986) [Differentiation of isolates of the Brazilian complex of bean
golden mosaic virus]. Fitopatologia Brasileira 11, 655-666.
Russell, D.R.; Wallace, K.M.; Bathe, J.H.; Martinell, B.J.; McCabe, D.E. (1993) Stable
transformation of Phaseolus vulgaris via electric-discharge mediated particle acceleration. Plant
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Schwartz, H.F.; Sanders, J.H. (1979) Plant diseases of dry beans in Latin America and strategies for
their control. CIAT, Cali, Colombia.
Shimizu, S.I.; Ikegami, M.; Fujii, H. (1987) Serological relationships between mung bean yellow
mosaic virus and other whitefly-transmitted geminiviruses. Journal of Agricultural Science, Tokyo
Nogyo Daigaku 32, 139-143.
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