horticultura brasileira Artigo convidado / Invited article

INOUE-NAGATA AK; LIMA MF; GILBERTSON RL. 2016. A review of geminivirus (begomovirus) diseases in vegetables and other crops in Brazil: current status and approaches for management. Horticultura Brasileira 34: 008-018. DOI - http://dx.doi.org/10.1590/S0102-053620160000100002 A review of geminivirus (begomovirus) diseases in vegetables and other crops in Brazil: current status and approaches for management Alice K Inoue-Nagata1; Mirtes F Lima1; Robert L Gilbertson2 1Embrapa Hortaliças, Brasília-DF, Brasil; [email protected]; [email protected]; 2UC Davis, Department of Plant Pathology, Davis, CA, USA; [email protected]

ABSTRACT RESUMO Insect-transmitted viruses cause some of the most damaging Uma revisão de geminiviroses (begomoviroses) em hortaliças and economically important diseases of crop plants, especially in e outras culturas: situação atual e estratégias de manejo tropical and subtropical regions. The geminiviruses, a group of Os vírus transmitidos por insetos causam algumas das doenças single-stranded DNA viruses with unique twined icosahedral virus mais severas e economicamente mais importantes em culturas particles, are responsible for many of these diseases. Of particular agrícolas, especialmente em regiões tropicais e subtropicais. Os importance are the geminiviruses transmitted by whiteflies Bemisia( geminivírus, um grupo único de vírus de DNA de fita simples com tabaci), which are in the genus Begomovirus. This is the largest partículas icosaédricas e geminadas, são responsáveis por muitas genus of plant viruses (in terms of number of species), and some dessas doenças. De particular importância são os geminivírus transmi- are responsible for devastating diseases in vegetable and fiber crops tidos por moscas-brancas (Bemisia tabaci), que pertencem ao gênero throughout the world. This review presents the current understanding Begomovirus. Esse é o maior gênero de vírus de plantas (em termos of begomoviruses, the diseases they cause, and approaches for de número de espécies), sendo que alguns dos begomovírus causam disease management. An emphasis is placed on the most important inúmeras doenças devastadoras em hortaliças e plantas produtoras begomovirus diseases in Brazil, which are those that affect common de fibras em todo o mundo. Esta revisão apresenta o conhecimento bean and tomato. However, because of the wide host range of the atual sobre os begomovírus, as begomoviroses e as estratégias de vector and the genetic flexibility of begomoviruses, these diseases manejo dessas doenças. Ênfase é colocada nas principais begomovi- pose a threat to many other crops. Therefore, the current situation roses que ocorrem no Brasil, que são aquelas que afetam o feijoeiro with begomoviruses that infect okra, pepper, potato, sweet potato e tomateiro. Entretanto, devido ao amplo círculo de hospedeiros do and soybean in Brazil is also discussed. vetor e da flexibilidade genética dos begomovírus, as begomoviroses representam ameaças a diversas culturas. Assim, discute-se também a situação atual das begomoviroses em batata, batata-doce, pimenta, quiabo e soja no Brasil.

Keywords: Bemisia tabaci, begomovirus, golden mosaic, integrated Palavras chave: Bemisia tabaci, begomovírus, mosaico dourado, pest management, whitefly. manejo integrado de pragas, mosca-branca.

General characteristics of mosaic in Africa; bean golden mosaic a twinned quasi-icosahedral virus geminiviruses (BGM) in the Americas; beet curly top particle (virion) that measures ~18 X The worldwide expansion of in North America and the Middle East; 30 nanometers and a small circular agriculture has also resulted in the cotton leaf curl in Asia; maize streak in single-stranded DNA genome of ~2.9- emergence and spread of numerous Africa; and tomato yellow leaf curl in 5.2 kilobases (kb). The family name is diseases and insect pests. Of particular Africa, the Americas, Asia and Europe. derived from the distinctive twinned importance are insect-transmitted In Brazil, BGM (Figures 1A, 2A) and virions (the Latin word gemini means viruses, especially in tropical and tomato diseases (Figures 1B, 2B, 2C) twin). Based upon genome structure, subtropical regions. Geminiviruses are caused by a complex of geminiviruses phylogenetic relationships, insect vector insect-transmitted viruses that have are important diseases that lead to and host range, seven genera have been emerged, over the past 20 years, as the substantial yield losses in common bean recognized: Begomovirus, Mastrevirus, largest group of plant viruses (in terms of and fresh market and processing tomato Curtovirus, Topocuvirus, Becurtovirus, number of species) and one of the most production. Turncurtovirus and Eragrovirus (Brown economically important. These viruses Geminiviruses comprise a et al., 2012). In nature, geminiviruses are cause extremely damaging diseases biologically and genetically diverse transmitted by phloem-feeding insects, in a wide range of crops throughout family (Geminiviridae) of viruses that including various species of leafhoppers, the world, including African cassava share the following characteristics: a treehopper and whiteflies of the

8 Hortic. bras., v. 34, n. 1, jan. - mar. 2016 A review of geminivirus (begomovirus) diseases in vegetables and other crops in Brazil: current status and approaches for management

species Bemisia tabaci (Figures 3A, et al., 2010) (although it has not been Brazil (Barbosa et al., 2015), and it may 3B). Geminiviruses are not transmitted reported so far in Brazil) and a complex be present in other parts of the country. through seeds, whereas many are graft- of sweet potato begomoviruses that are Effective management of B. tabaci transmissible and some are mechanically widespread in Brazil and other NW is difficult. The most common control (sap) transmissible. Plants infected with regions (Albuquerque et al., 2012a). In method is the application of insecticides, geminiviruses show a wide range of addition, indigenous NW monopartite mostly combinations of neonicotinoids, symptoms including stunting, distorted tomato-infecting begomoviruses have juvenoids and growth regulators. These growth, and leaf streaking and striations been recently identified, e.g., Tomato materials target different stages of the in monocotiledonous plants and leaf leaf deformation virus (ToLDV) in insect, i.e., eggs, nymphs or adults, crumpling, curling, distortion, golden- Peru and Tomato mottle leaf curl virus whereas others block feeding of the light green-yellow mosaic/mottle, (ToMoLCV; Figure 2B) in Brazil insect. Targeting only adults may be one interveinal yellowing, yellow spots, and (Gilbertson et al., 2015). In general, reason for the low control efficiency in vein swelling, purpling, and yellowing begomoviruses cause similar symptoms some situations. Hence, it is important in dicotyledonous plants. in plants, including stunting and leaf to monitor fields and be aware of the distortion and some combination of insect stage(s) present before selecting Emergence of whitefly-transmitted golden-light green-yellow mosaic/ the insecticide to be applied. Dosage geminiviruses (begomoviruses) mottle, crumpling, curling, distortion, and application volume, mode and veinal or interveinal yellowing, and The whitefly-transmitted timing are other factors that strongly yellow spots in leaves. Identification of geminiviruses are in the genus influence the efficiency of insecticide a specific begomovirus requires the use Begomovirus. They comprise the largest control of whiteflies. In addition, the of molecular methods (e.g., rolling circle number of species (288 of 325 total constant and repeated use of the same amplification [RCA], polymerase chain species) in the family Geminiviridae active ingredient favors the selection reaction [PCR] and sequencing). (Brown et al., 2012), and will be the and multiplication of individuals that focus of this review. The remarkable are resistant to that specific chemistry. emergence of these viruses has been The whitefly vector of Indeed, it is common to hear growers driven by the B. tabaci vector, especially begomoviruses complaining that a certain insecticide the polyphagous biotype B that has The vector of begomoviruses, no longer kills whiteflies or that a spread throughout the world (Gilbertson B. tabaci (Figure 3), is a complex higher dose is needed to be effective; et al., 2015). Begomoviruses can be of morphologically similar, but this suggests the selection of a resistant subdivided into two major groups: biologically and genetically distinct population, often due to excessive bipartite viruses, those with a genome populations. The species B. tabaci is and repeated spraying of the same composed of two ~2.6 kb DNA divided into biotypes (e.g., A, B, Q), chemical. Finally, the complexity components (referred to as DNA-A which are probably distinct enough to of the Brazilian agricultural system and DNA-B), which are prevalent in the be considered as species (de Barro et contributes to the difficulty in controlling New World (NW, e.g., southern states al., 2011). This has led to a proposal whiteflies. BecauseB. tabaci biotype B of the United States of America (USA), to elevate some biotypes to the species is highly polyphagous, they reproduce Mexico, the Caribbean and Central level, including NW (biotype A), on numerous crops, weeds and non- and South America); and monopartite Middle East-Asian Minor 1 (biotype cultivated plants. Thus, in irrigated viruses, those with a genome composed B) and Mediterranean (biotype Q), agricultural production systems, crop of a single ~2.9 kb genomic DNA, which based on their inability to interbreed hosts of the whitefly are always present are prevalent in the Old World (OW, and divergence in the mitochondrial and act as bridges to maintain B. tabaci e.g., Europe, Africa, Asia and Australia). cytochrome oxidase 1 (mtCO1) gene populations throughout the year. For Many monopartite begomoviruses (de Barro et al., 2011). However, for this example, overlapping of soybean, are associated with satellite DNAs review, we will use biotype designations cotton, potato, tomato, and bean crops in (alphasatellites and betasatellites), some as they are more familiar and most Brazil provides continual host plants for of which enhance pathogenicity (Zhou, commonly used in the literature. In whiteflies in many regions. Whiteflies 2013). The bipartite and monopartite Brazil, biotype B is currently the prefer hot and dry periods, therefore begomoviruses reflect an ancestral predominant biotype. Biotype A is high populations are seen usually from division that possibly occurred before believed to have been prevalent prior December to March, particularly in the continental drift. However, more to the introduction of biotype B in the ‘veranico’ period (periods of at least two weeks without rain in the summer recently the boundaries between these 1990’s. Like in other geographical or wet season). two groups have become less clear. areas, biotype B rapidly displaced This is because of the introduction the indigenous biotype(s). Today, and establishment of OW monopartite the B. tabaci biotype B is distributed Begomovirus diseases in Brazil begomoviruses into the NW, e.g., throughout Brazil. Recently, the biotype The most important begomovirus Tomato yellow leaf curl virus (TYLCV) Q, which possesses resistance to certain diseases in Brazil are BGM (Figure in many regions of the NW (Lefeuvre insecticides, was reported in the south of 1A) and a number of diseases of tomato

Hortic. bras., v. 34, n. 1, jan. - mar. 2016 9 AK Inoue-Nagata et al.

(Figure 1B) caused by a complex of associated with massive increases of stabilizing selection and is well adapted viruses. In situations where whitefly whitefly populations that developed on to the common bean host. In addition populations are high and bean or tomato vast acreages of soybean. Epidemics to BGMV, other begomoviruses can crops are infected with these viruses of BGM in Brazil typically occur infect common bean in Brazil, such early in development, entire fields can during hot dry weather in the summer as Macroptilium yellow spot virus be destroyed or abandoned due to these months, as well as in dry periods, known (MaYSV), which induces yellow diseases (Figure 1B). Other crops (e.g., as ‘veranico’, that occur during the spotting, leaf crumpling and distortion okra, pepper, potato and sweet potato) rainy season. The occurrence of BGM (Ramos-Sobrinho et al., 2014). MaYSV can be infected by begomoviruses in epidemics has fluctuated over the past occurs in the North-East region of the Brazil, but economic losses are not decade, but the disease remains a major country. Recently, an isolate of Sida substantial or widespread. Weeds in concern for growers. For example, as micrantha mosaic virus (SiMMV), Brazil are commonly infected with recently as 2013, epidemics of BGM a weed infecting begomovirus, was begomoviruses and often show striking in the major bean producing regions reported infecting common bean in the light green, golden or yellow mosaic caused substantial economic losses (G1 state of Goiás, where it was associated symptoms (Figure 2F), and these can Globo, 2013). with golden mosaic, chlorotic spots serve as progenitors for new crop- Unlike tomato begomovirus diseases and leaf distortion (Fernandes-Acioli infecting begomoviruses (Rocha et al., in Brazil, which emerged following the et al., 2011). 2013). introduction of the B. tabaci biotype In Mexico and countries of Central Finally, whereas begomoviruses B in the 1990s, outbreaks of BGM America, BGM is also one of the most are the major and perhaps the only were driven by indigenous B. tabaci important diseases of common bean. type of geminivirus found in Brazil, populations, presumably biotype A. Here, the disease is caused by a different it is worth noting that a disease with This indicated that the biotype A was an bipartite begomovirus species, Bean symptoms similar to the curly top of effective vector ofBean golden mosaic golden yellow mosaic virus (BGYMV), sugar beets and vegetable crops that virus (BGMV) and probably of other with biological (sap transmission and occurs in the western USA and Asia begomoviruses, given the extensive virulence on bean germplasm) and (Iran and Turkey) has been reported infection of weeds with a diversity of genomic (DNA sequence) properties in Argentina and Brazil (Costa, 1952). begomoviruses prior to the introduction that are different from those of BGMV Although this disease was demonstrated of biotype B in the country. Furthermore, (Faria et al., 1994). This was one to be leafhopper-transmitted, the causal BGM outbreaks continued following the of the first examples of genetically agent has not been characterized. This displacement of biotype A by biotype distinct begomovirus species causing disease has not been observed in Brazil B, indicating that both biotypes are the same type of disease in a crop plant for many years, indicating that it is not effective vectors of BGMV. This is (Gilbertson et al., 1993). This local or economically important. despite the fact that, in general, beans parallel evolution of genetically distinct In this review, the major and minor are less preferred hosts of B. tabaci begomoviruses causing a similar disease diseases caused by begomoviruses in in Brazil compared with cucurbits, has proven to be a common phenomenon vegetables and other crops in Brazil soybeans, brassicas or tomatoes. in the evolution of begomoviruses (Table 1) are described. In addition, However, because begomoviruses are (Gilbertson et al., 2015). Sources of the approaches and challenges faced transmitted in a persistent circulative resistance have been identified for by growers in managing these diseases manner by B. tabaci, low populations BGYMV and cultivars with some are discussed. of viruliferous whiteflies can lead to a degree of resistance have been released high incidence of infection in the field. in Central America and Mexico. Thus, the greatest yield losses due to Beans (Phaseolus vulgaris) The continuing epidemics of BGM BGM occur when there are high rates BGM has been one of the most in Brazil demonstrate that effective of infection early in the growing season, damaging diseases of common beans disease management remains a and this is not necessarily correlated (and to a lesser extent, lima beans) challenge. Resistant cultivars are not with the highest populations of B. in Brazil since it emerged in the commercially available, which reflects a 1960s (Costa, 1965). The disease is tabaci. lack of sources of resistance to BGMV in characterized by a striking golden- The, causal agent of BGMV is a Phaseolus germplasm. Management of yellow mosaic/mottle of leaves, as well typical NW bipartite begomovirus whitefly populations with insecticides is as blistering, chlorosis, crumpling, and (Table 1; Gilbertson et al., 1993). It is the often not effective, due to the efficiency rugosity (Figures 1A, 2A). Infected predominant begomovirus associated with which whiteflies transmit the plants are often stunted, particularly with BGM in Brazil and Argentina virus and the difficulties in controlling when infected early in development, (Faria et al., 2000). Genetic studies large populations in different crops and and yields can be substantially reduced. have revealed a low level of genetic weeds. BGM was the first begomovirus disease diversity among BGMV isolates in One approach that can be effective is that reached epidemic levels in the Brazil (Faria & Maxwell., 1999), which the implementation of a bean-free period NW. In Brazil, these epidemics were indicates that the virus has undergone [IN 15, SDA, Ministry of Agriculture,

10 Hortic. bras., v. 34, n. 1, jan. - mar. 2016 A review of geminivirus (begomovirus) diseases in vegetables and other crops in Brazil: current status and approaches for management

Livestock and Food Supply (MAPA), hosts (e.g., soybean, tomato and potato) least 14 distinct indigenous tomato- Jun 16, 2014], in which growing beans during this period, it appears that it is infecting begomoviruses emerged is prohibited for a one month period a useful management strategy for the locally following the introduction of B. on a regional basis. For this regulation, disease in Brazil. tabaci biotype B. the major bean growing regions in Due to the lack of Phaseolus The first tomato begomovirus disease central Brazil, which are most severely germplasm with conventional in Brazil was tomato golden mosaic affected by BGM, were divided into two resistance to BGMV, a transgenic (TGM), which was reported in the sub-regions: region 1, comprising the approach has been used to engineer 1960’s (Costa, 1976). The disease was municipalities located in the southern resistance into common bean (Bonfim characterized by distorted growth and a part of the state of Goiás, where the et al., 2007). Here, a gene silencing yellow to light green mosaic of leaves, bean-free period is implemented from (RNA interference) strategy, in which a and it was shown to be transmitted by September 5 to October 5; and region construct designed to express a double- whiteflies. As with BGM, it is believed 2, comprising the northern part of stranded RNA (dsRNA) corresponding that TGM was transmitted by the Goiás, the Minas Gerais State and the to a portion of the viral gene encoding indigenous B. tabaci biotype A but, Federal District, where the free period the replication-associated protein (Rep) in contrast to the situation with BGM,

is between September 20 to October 20. was transformed into common bean TGM never reached high incidences This approach takes advantage of the plants. The expression of the dsRNA or caused substantial economic losses. narrow host range of BGMV (primarily triggers silencing of the viral mRNA The causal agent of TGM is Tomato common bean and lima bean) and the encoding the Rep, which greatly reduces golden mosaic virus (TGMV; Matyis fact that the virus is not transmitted to the viral replication. These transgenic et al., 1975), a typical NW bipartite progeny of the whitefly vector. Recent plants [Brazilian Agricultural Research begomovirus. Although TGMV results with a BGMV agroinoculation Corporation (Embrapa) 5.1 event] are never emerged as an economically system has confirmed the narrow host highly resistant to BGMV infection important virus, it was one of the first range of BGMV, and supported the use (Aragão et al., 2013). After many years begomoviruses to be characterized on of a bean-free period as a recommended of greenhouse and field testing, followed the molecular level and it played a key BGM management strategy. Thus, by biosafety evaluations, these BGMV- role in studies establishing that some following the host-free period, the resistant transgenic beans were approved begomoviruses possess a bipartite inoculum level of the virus is reduced for commercial release in 2011. It is genome and a number of aspects of and, hopefully, the whitefly population expected that seeds of this transgenic viral gene expression and function (e.g., as well. A similar approach has been bean cultivar will be available for Hamilton et al., 1983). Ironically, these effectively used to manage BGM caused purchase beginning in 2016. However, pioneering experiments with TGMV by BGYMV in the Dominican Republic. growers must be aware that the use of were performed in the laboratory host, After the epidemics of BGM in the transgenic cultivar represents only Nicotiana benthamiana, and it was 2013 (G1 Globo, 2013), when growers one strategy for disease management not until many years later that Koch’s experienced substantial losses, there was of BGM, and that this transgenic bean Postulates were fulfilled with TGMV a strong pressure for a response from cultivar is not resistant to other bean- in tomato, i.e., reproducing TGM the Brazilian Ministry of Agriculture. infecting viruses, including the whitefly- symptoms in tomato with infectious Meetings were held on the local, transmitted Cowpea mild mottle virus DNA-A and DNA-B clones of the virus regional and national levels, and a plan and, possibly, MaYSV and SiMMV. (Wyant et al., 2012). for the implementation of a mandatory Thus, other control measures, as part of It is believed that one of the reasons bean-free period was agreed upon. Still an integrated pest management (IPM) that TGM never became an economically program (Gilbertson et al., 2011), are controversial in many regions, the bean- important disease in Brazil was that needed for effective management of free period described in the previous tomato was not a preferred host for BGM. paragraph was first implemented in the B. tabaci biotype A. The situation Federal District in 2013, followed by with tomato begomoviruses in Brazil the states of Goiás and Minas Gerais Tomato (Solanum lycopersicum) changed dramatically following the in 2014. Growers report that since the Tomato begomoviruses represent introduction of the biotype B, which is implementation of the bean-free period, one of the major constraints on tomato highly polyphagous and feeds on tomato, the incidence of BGM has been reduced production in tropical and subtropical as well as many other crops and non- substantially (Canal Rural, 2015). regions of the world. Under high cultivated plants (e.g., weeds). Indeed, Therefore, most growers seem to be whitefly pressure, yield losses can be as this ‘supervector’ of plant viruses convinced that the bean-free period is high as 100%. Due to the phenomenon drove the emergence of new species an effective management strategy for of local evolution, more than 60 species of tomato-infecting begomoviruses BGM, although some remain skeptical. of tomato-infecting begomoviruses have in Brazil (Table 1) and in many other Thus, despite some of the challenges been described worldwide. Indeed, regions of the world (Gilbertson et in implementing the bean-free period the situation in Brazil is an excellent al., 2015). Moreover, in contrast to and the presence of other whitefly example of this phenomenon, as at the situation in the Caribbean, Mexico Hortic. bras., v. 34, n. 1, jan. - mar. 2016 11 AK Inoue-Nagata et al. and the southeastern USA, where the tomato cultivars with resistance to November. This allows for an annual invasive OW monopartite TYLCV has tomato-infecting begomoviruses are tomato-free period of at least two emerged as the predominant tomato- commercially available. These cultivars months (December and January). infecting begomovirus (Lefeuvre et al., are hybrids and possess one or more The tomato-free period appears to 2010), the viruses emerging in Brazil of the begomovirus resistance genes be having a positive effect, delaying were unique and emerged from the Ty-1, Ty-2, Ty-3, Ty-4, Ty-5, ty-5, tcm- the appearance of the virus (helping large and genetically diverse reservoir 1, and tgr1. In general, the currently avoid early infections when plants are of indigenous begomoviruses infecting available hybrids are moderately most susceptible) and reducing overall noncultivated plants (weeds) (Rocha et resistant, i.e., they become infected disease incidence. For this reason, al., 2013). and show mild symptoms of light green the tomato-free period is generally To date, at least 14 recognized species mosaic and crumpling of leaves, but accepted by the processing tomato of tomato-infecting begomoviruses have they provide acceptable yields in areas industry and it is being implemented been described from Brazil (Ribeiro where begomovirus disease pressure non-officially in other states. Challenges et al., 2003; Fernandes et al., 2006; is high, e.g., states of Goiás, Minas to the effectiveness of the tomato-free Castillo-Urquiza et al., 2008; Barbosa Gerais, Ceará, and São Paulo. It is also period include continuous cropping of et al., 2011; Albuquerque et al., 2012b; important to emphasize that different indeterminate fresh market tomatoes, Rocha et al., 2013). The disease begomovirus resistance genes do not which serve as an inoculum source symptoms induced by these viruses confer a similar level of resistance to throughout the year, and the apparently include stunting and distorted growth all begomovirus(es); thus, it is critical wider host range of some tomato- and golden-light green-yellow mosaic/ to evaluate resistant cultivars for their infecting begomoviruses. For example, mottle, crumpling, curling, interveinal response to the begomoviruses prevalent recent studies have shown that ToSRV chlorosis, rugosity, vein yellowing and in a given region before widespread can cause a symptomless infection in purpling, and yellow spotting in leaves deployment. For example, in Brazil, beans (which can be grown during the (Figures 1B, 2B, 2C). Because these cultivars with Ty1/Ty3 genes tend to be tomato-free period) and that whiteflies viruses cause similar symptoms in resistant, whereas those with the Ty2 can acquire the virus from such plants. infected tomato plants, molecular tools gene are not. It is likely that cultivars However, when used as part of an IPM (RCA, PCR and sequencing) are needed with even higher levels of resistance strategy, the tomato-free period is a very for precise identification. Application of will become available in the future. effective management strategy. these tools to study Brazilian tomato- In Brazil, as in many other tomato- The worldwide spread of the B. infecting begomoviruses has revealed growing regions of the world, it will tabaci biotype B and plant materials has that two viruses are prevalent: Tomato also be important to combine resistance allowed for the long-distance spread of severe rugose virus (ToSRV, Figure 2C) to begomoviruses and tospoviruses, begomoviruses to new areas (Gilbertson and ToMoLCV (Figure 2B). ToSRV as the latter are also emerging as et al., 2015). This is exemplified by the is prevalent in central-to-southern major constraints on tomato production aggressive TYLCV, which has become tomato growing regions (e.g., the (Gilbertson et al., 2015). established throughout the NW and Federal District and states of Minas A second management strategy that causes severe symptoms of stunting, Gerais, São Paulo and Goiás), whereas can be very effective for tomato-infecting leaf curling, yellowing and substantial ToMoLCV is most common in the begomoviruses is the implementation of yield loss. Fortunately, TYLCV has not north-eastern regions (e.g., the states a tomato- or whitefly host-free period. yet been detected in Brazil and efforts of Ceará, Piauí and the northern part of The underlying basis for the success to prevent the introduction of this virus Minas Gerais). Interestingly, although of this approach is the same as that should be a priority (e.g., not allowing most of these viruses are typical NW described for BGM (narrow host range importation of tomato transplants). In bipartite begomoviruses, recent studies of the virus and no transmission of the some countries, such as the Dominican of ToMoLCV have established that it is virus to the progeny of the whitefly Republic, effective management of another example of an indigenous NW vector). In 2003, a tomato-free period TYLCV has been accomplished through monopartite begomovirus (Gilbertson of two months was established for the use of a three month whitefly- et al., 2015). Thus, as in many other the processing tomato industry by the host free period, planting of resistant parts of the world, the invasive B. tabaci Ministry of Agriculture in Brazil (IN cultivars (especially late in the season), biotype B has driven the emergence 024, SDA, MAPA, April 15, 2003). whitefly management and sanitation, of a diversity of new-tomato infecting The tomato-free period was officially e.g., prompt removal or destruction begomovirus species via local evolution implemented in the state of Goiás, of plants after harvest (Salati et al., in Brazil. beginning in 2007 [IN 05/2007; IN 2002). This IPM strategy has proved Management of diseases caused 06/2011, Goiás Agency for Agriculture to be effective for management of by tomato-infecting begomoviruses and Livestock Defense (Agrodefesa)]. TYLCV and prevented the elimination in Brazil requires an IPM strategy Tomatoes can be transplanted only of the processing tomato industry in the (Gilbertson et al., 2011). Unlike the from February 1 to June 30 and harvest Dominican Republic. In Brazil, although situation in common bean with BGMV, must be completed by the end of the implementation of a whitefly host-

12 Hortic. bras., v. 34, n. 1, jan. - mar. 2016 A review of geminivirus (begomovirus) diseases in vegetables and other crops in Brazil: current status and approaches for management free period is extremely difficult due to ToYVSV and ToSRV (Souza-Dias et first report of a begomovirus infecting the overlapping cultivation of whitefly al., 2008; Lima et al., 2011; Lima & sweet pepper in Brazil was in 2001 (Lima hosts (beans, soybeans, cotton, tomatoes Vieira, 2015). As ToYVSV and ToSRV et al., 2001) and, in chili pepper, in 2006 and potatoes) in many of the main primarily infect tomatoes, it is believed (Bezerra-Agassie et al., 2006) when a C. agricultural areas, it can be helpful as that tomato plants are the major source baccatum plant with symptoms of virus part of an IPM strategy, as discussed in for potatoes. Indeed, it was shown that infection was collected in a survey in the previous paragraph. ToYVSV was transmitted to potato the state of Goiás, in 2003. Symptoms plants by whiteflies after short periods of in this plant resembled those caused Potato (Solanum tuberosum) vector feeding on infected tomato plants by begomovirus infection in other Potato is one of the most important (Souza-Dias et al., 1996). hosts, e.g., chlorotic spots, rugosity, crops in Brazilian agriculture. The Although begomovirus diseases and mild leaf distortion (Figure 2E), production is concentrated in the have been detected in some of the main and the bipartite begomovirus ToSRV Southeast (e.g., states of Minas Gerais potato producing regions of the country was detected. Tomato golden vein virus and São Paulo), South (e.g., states of (Table 1), they occur at low incidences. and ToYVSV have also been reported Paraná and Rio Grande do Sul) and However, as potato is a vegetatively- in pepper plants in Brazil (Nozaki et Central-West (e.g., state of Goiás) propagated crop, a major concern is that al., 2010). In C. annuum, yield losses regions of the country. In Brazil, potato begomoviruses may be translocated to of 28-45% have been attributed to has been affected by different viral tubers, producing infected seed tubers, begomovirus infection indicating the diseases causing mainly mosaic and leaf resulting in rapid virus spread and tubers potential importance of such diseases rolling symptoms (e.g., Potato virus Y - with reduced quality. Lima et al. (2012) in Brazil. At present, no Capsicum PVY - and Potato leafroll virus - PLRV), observed virus transmission rates as spp. germplasm with resistance to which often result in yield losses. high as 80-100% in tubers obtained begomoviruses is available. Whitefly-transmitted begomoviruses from begomovirus-infected potato Whereas diseases caused by other have been reported to infect potato in plants. Together with increased whitefly viruses are clearly more important many regions of the world. However, populations on potatoes in tropical and in pepper in Brazil (e.g., potyviruses to date, diseases caused by these viruses subtropical production regions of Brazil, such as Pepper yellow mosaic virus), have not been a major problem for the potential exists for begomoviruses it should be noted that pepper-infecting potato production in most regions. to become a more important problem begomoviruses are very important and In Brazil, begomovirus diseases of for potato production. Moreover, as cause substantial yield losses in other potato are not widespread in the main little is known of the epidemiology areas of the world, including Mexico production regions and generally occur of begomovirus diseases of potato in and Central America in the NW and at low incidences (Table 1). Brazil, it is important to monitor potato Asia (especially India) and Africa in the The first report of a potato-infecting production areas for whiteflies and OW. Mixed infections of begomoviruses begomovirus in Brazil was made in begomovirus disease incidence and and aphid-transmitted viruses are the 1980’s in the state of Rio Grande species in case these diseases become also prevalent in these regions. This do Sul. The disease was referred to more important. demonstrates that pepper can be a as deforming mosaic. Later, it was suitable host for B. tabaci populations shown that the disease was caused by Pepper (Capsicum spp.) in other regions of the world, and that an isolate of Tomato yellow vein streak Pepper is an important crop in the insect vector is not genetically virus (ToYVSV), which induces yellow Brazil. There is a high level of genetic homogenous, at least in terms of host mosaic and leaf distortion symptoms in diversity in the types of pepper grown, preference. Thus, the emergence potatoes (Ribeiro et al., 2006). When the and fruits come in a wide range of of begomoviruses as economically disease was first observed, the incidence shapes, sizes, colors and pungency. The important viruses of pepper in Brazil is a was low (3%) and no economic losses predominant species cultivated in Brazil possibility, and pepper fields in different were reported. In subsequent surveys, are Capsicum annuum, C. frutescens, C. growing regions of Brazil should be losses as high as 25-40% were attributed chinense and C. baccatum. monitored for whitefly populations and to begomovirus infection in some potato In general, pepper plants are a appearance of unusual virus symptoms. fields, indicating that the disease was poor host of B. tabaci in Brazil, spreading and started representing a and other crops such as tomatoes are Sweet potato (Ipomoea batatas) potential threat to potato production preferred when grown side-by-side. Sweet potato is a vegetatively (Daniels, 1985). More recently, yellow Consistent with the non-preference of propagated crop, and planting of virus- mosaic disease symptoms (Figure 2D) whiteflies for pepper, diseases caused infected cuttings is a serious problem have re-emerged as a problem on potato by begomoviruses in pepper are not that can lead to high levels of infection, in the central-to-south potato producing prevalent or economically important in as well as losses in yield and quality. regions (e.g., states of Goiás, São Paulo, Brazil. However, over the last decade, In general, sweet potato plants are Minas Gerais and the Federal District), the incidence of begomovirus infection commonly infected by multiple viruses and have been shown to be caused by in peppers in Brazil has increased. The in the field, including RNA viruses such

Hortic. bras., v. 34, n. 1, jan. - mar. 2016 13 AK Inoue-Nagata et al. as criniviruses and potyviruses, and begomovirus infection in sweet potato infecting sweet potato plants throughout DNA viruses such as begomoviruses. based upon symptoms is very difficult, the world, and the presence of some Begomovirus symptoms in sweet potato and molecular methods are needed for of these viruses in sweet potato plants include leaf curling, crumpling and definitive identification. from multiple continents suggests vein yellowing. However, diagnosis of Begomoviruses have been detected long-distance spread in association

Table 1. Geminivirus species reported on vegetable and other crops in Brazil, and recognized by the International Committee on Taxonomy of Viruses (espécies de geminivírus relatadas em hortaliças e outras culturas no Brasil e reconhecidas pela Comissão Internacional de Taxonomia de Vírus). Brasília, Embrapa Vegetables, 2015. Crop Acronym Species Type Importance BGMV Bean golden mosaic virus Bipartite Major importance, widespread Beans MaYSV Macroptillium yellow spot virus Bipartite Important in North-East SiMMV Sida micrantha mosaic virus Bipartite Important in weeds, widespread OMoV Okra mottle virus Bipartite Minor importance, one report Okra SiMMV Sida micrantha mosaic virus Bipartite Important in weeds, widespread TGVV Tomato golden vein virus Bipartite Minor importance Pepper ToSRV Tomato severe rugose virus Bipartite Major importance, widespread ToYVSV Tomato yellow vein streak virus Bipartite Minor importance ToSRV Tomato severe rugose virus Bipartite Widespread, potentially important Potato ToYVSV Tomato yellow vein streak virus Bipartite Minor importance BGMV Bean golden mosaic virus Bipartite Widespread, but minor importance SiMMV Sida micrantha mosaic virus Bipartite Minor importance, one report Soybeans SiMoV Sida mottle virus Bipartite Minor importance, one report SoCSV Soybean chlorotic spot virus Bipartite Minor importance, one report MerLCV Merremia leaf curl virus Monopartite Minor importance, one report SPGVV Sweet potato golden vein virus Monopartite Minor importance, one report SPLCBRV Sweet potato leaf curl Brazil virus Monopartite Minor importance, one report Sweet po- SPLCLaV Sweet potato leaf curl Lanzarote virus Monopartite Minor importance, one report tato SPLCESP Sweet potato leaf curl Spain virus Monopartite Minor importance, one report SPLCSPV Sweet potato leaf curl Sao Paulo virus Monopartite Minor importance, one report SPLCV Sweet potato leaf curl virus Monopartite Major importance SPMV Sweet potato Malaga virus Monopartite Minor importance, one report SiMMV Sida micrantha mosaic virus Bipartite Minor importance SiMoV Sida mottle virus Bipartite One report TGMV Tomato golden mosaic virus Bipartite Not detected any more TGVV Tomato golden vein virus Bipartite Minor importance TMiMV Tomato mild mosaic virus Bipartite Minor importance, one report ToCmMV Tomato common mosaic virus Bipartite Minor importance ToCMoV Tomato chlorotic mottle virus Bipartite Minor importance Tomato ToICV Tomato interveinal chlorosis virus Bipartite Minor importance, one report ToLDV Tomato leaf distortion virus Bipartite Minor importance, one report Major importance, especially in ToMoLCV Tomato mottle leaf curl virus Monopartite North-East ToRMV Tomato rugose mosaic virus Bipartite Not detected any more ToSRV Tomato severe rugose virus Bipartite Major importance, widespread ToYSV Tomato yellow spot virus Bipartite Minor importance ToYVSV Tomato yellow vein streak virus Bipartite Minor/local importance

14 Hortic. bras., v. 34, n. 1, jan. - mar. 2016 A review of geminivirus (begomovirus) diseases in vegetables and other crops in Brazil: current status and approaches for management

with propagative materials (cuttings planting material. Malvaceous weeds. The symptoms and roots). Indeed, evidence of the induced in okra by these begomoviruses importance of propagative materials Okra (Abelmoschus esculentus) were mild mottling and chlorotic spots. as a means of spread for these viruses It is not believed that these viruses Okra (family Malvaceae) is typically comes from the observation that many reach high incidences of infection or grown by smallholder farmers in Brazil. of them are inefficiently transmitted by cause economic losses in okra and, thus, A number of other Malvaceous crops whiteflies. In Brazil, eight begomovirus may be spill over from infected weeds. are grown in Brazil, most notably species have been reported from sweet As these viruses infect other plants, cotton, but also hibiscus. In addition, potato including Sweet potato leaf curl including common bean, soybean and numerous Malvaceous weeds (e.g., virus (SPLCV), Sweet potato golden weeds, it is possible that okra plays a Malva spp. and Sida spp.) can be found vein virus (SPGGV), Sweet potato role as a reservoir in some agricultural throughout Brazil, and often show leaf curl Spain virus (SPLCESV), ecosystems. symptoms of begomovirus infection Sweet potato leaf curl Sao Paulo virus, (e.g., yellow mosaic and mottle). Merremia leaf curl virus, Sweet potato However, begomovirus diseases have Soybean (Glycine max) leaf curl Brazil virus, Sweet potato not emerged as economic problems in Soybeans are extensively grown Lanzarote virus and Sweet potato okra (or cotton or hibiscus). The reason in Brazil and are one of the most Malaga virus (Paprotka et al., 2010; for this is not clear, as these plants are important agricultural commodities. Albuquerque et al., 2011, 2012a). The hosts of whiteflies (especially cotton), Planting is usually done between genome of these viruses is monopartite and a diversity of begomoviruses infect October and December and the harvest and most similar to those of OW Malvaceous weeds, and these could is from January to April. Soybeans are begomoviruses. Together with reports serve as progenitors for begomoviruses a preferred host of B. tabaci, and heavy of some of these viruses from OW infecting Malvaceous crops in Brazil. infestations can be observed in soybean locations, it is likely that these viruses In the past, a disease known as okra fields, particularly in hot and dry periods or their progenitors were introduced mosaic was reported in Brazil, and (summer months and 'veranico' periods). into Brazil on multiple occasions in the causal agent was believed to be a Growers typically do not manage association with propagative materials. begomovirus. However, the disease whitefly populations in soybean as it is No information is available regarding was apparently effectively controlled believed that this insect causes little or begomovirus-resistant germplasm and by the use of resistant varieties. Thus, it no yield loss. In some cases, growers yield losses caused by these viruses in is possible that okra plants are resistant may try to control whiteflies late in Brazil. The use of virus-free propagative to the major begomoviruses in Brazil. the growing season to prevent damage materials is the best way to control Two begomoviruses have been reported from sooty mood, but this is usually sweet potato viruses. For this reason, infecting okra plants in Brazil, SiMMV unsuccessful. Although begomovirus many countries have clean stock (Aranha et al., 2011) and Okra mottle diseases are not economically important, programs, based on eliminating viruses virus (OMoV) (Albuquerque et al., soybeans can be infected with a number via meristem tip culture, for providing 2013). Not surprisingly, the source of of begomoviruses, such as BGMV, growers with virus-free sweet potato these viruses was believed to be infected SiMMV, Sida mottle virus and Soybean

A B

Figure 1. Fields with 100% incidence of begomovirus disease. (A) A common bean field withBean golden mosaic virus (BGMV), and (B) a tomato field withTomato severe rugose virus (ToSRV) {lavouras com 100% de incidência de begomoviroses. (A) Lavoura de feijão com o Bean golden mosaic virus (BGMV), e (B) Lavoura de tomate com o Tomato severe rugose virus (ToSRV)}. Brasília, Embrapa Vegetables, 2015.

Hortic. bras., v. 34, n. 1, jan. - mar. 2016 15 AK Inoue-Nagata et al.

A B C

D E F

Figure 2. Begomovirus disease symptoms. (A) Common bean infected with BGMV; (B) tomato infected with Tomato mottle leaf curl virus (ToMoLCV) and (C) Tomato severe rugose virus (ToSRV); (D) potato and (E) pepper with symptoms of begomovirus infection, and; (F) Nicandra physaloides infected with ToSRV {sintomas de begomoviroses. (A) Feijoeiro infectado por BGMV; (B) tomateiro infectado pelo Tomato mottle leaf curl virus (ToMoLCV) e (C) pelo Tomato severe rugose virus (ToSRV); (D) batateira e (E) pimenteira com sintomas de infecção por begomovírus e; (F) Nicandra physaloides infectada por ToSRV}. Brasília, Embrapa Vegetables, 2015.

whitefly management efforts have been A B implemented. Such programs would directly benefit soybean growers, as well as indirectly benefit growers of other crops, by reducing the multiplication of whiteflies that migrate out in clouds to other plants.

Concluding remarks What should be clear from this review is that the begomovirus situation in Brazil has many characteristics that are unique, including the viruses involved (mostly locally evolved) and the crops most heavily impacted (beans and tomato). The lack of begomovirus disease problems in crops such as cotton, okra and pepper, which are heavily impacted by such diseases in other parts of the world, likely reveals differences in properties of the virus progenitors Figure 3. Adult of whiteflyBemisia tabaci (A) and a tomato leaf infested by adult whiteflies in noncultivated plants (weeds) and (B) {adulto da mosca branca Bemisia tabaci (A) e uma folha de tomateiro infestada por adultos da mosca branca (B)}. Brasília, Embrapa Vegetables, 2015. the whitefly (host preference). The overlapping and extensive cropping of preferred whitefly hosts in Brazil chlorotic spot virus (Table 1; Coco et al., disease pressure it is possible that (beans, soybeans, cotton and tomato) 2013; Fernandes et al., 2009). Symptoms yield losses could occur and that this also presents unique challenges for of begomovirus infection in soybean could justify a program for managing effective and sustainable management include stunting, distorted growth and viruses and whiteflies. Recently, some of begomovirus diseases. On the other blistering, chlorotic spots, and light soybean growers have become aware hand, a factor common to Brazil and green to golden-yellow mosaic/mottling of the risk posed by begomovirus other regions of the world has been the of leaves. Thus, under high begomovirus diseases in soybean production and introduction and establishment of the

16 Hortic. bras., v. 34, n. 1, jan. - mar. 2016 A review of geminivirus (begomovirus) diseases in vegetables and other crops in Brazil: current status and approaches for management

B. tabaci B biotype (Figure 3) and the populations with insecticides will virus arose from a double recombination event. subsequent emergence of economically continue to be an important tool, but Archives of Virology 158: 181-186. important diseases caused by tomato- it should be done based on IPM, i.e., ALBUQUERQUE LC; INOUE-NAGATA AK; PINHEIRO B; RESENDE RO; MORIONES infecting begomoviruses (Table 1). only when populations reach defined E; NAVAS-CASTILLO J. 2012a. Genetic Following the introduction of the thresholds and using rotation of different diversity and recombination analysis of biotype B into Brazil, many factors have chemistries. The availability of new sweepoviruses from Brazil. Virology Journal contributed to the spread and build-up of and improved chemistries for whitefly 9: 241. ALBUQUERQUE LC; INOUE-NAGATA AK; populations and the level of damage they management should allow for better PINHEIRO B; RIBEIRO SG; RESENDE RO; cause. These include irrigation; intensive management, but it will be important MORIONES E; NAVAS-CASTILLO J. 2011. cultivation and monoculture of preferred to facilitate the registration of these A novel monopartite begomovirus infecting host plants (beans, soybeans, cotton, materials in a timely manner so they sweet potato in Brazil. Archives of Virology 156: 1291-1294. potato and tomato) throughout the will be available to growers in Brazil. ALBUQUERQUE LC; VARSANI A; year; greenhouse cultivation, resulting Unfortunately, biological control of FERNANDES FR; PINHEIRO B; MARTIN in whitefly propagation during cold whiteflies in open fields is not effective DP; FERREIRA PTO; LEMOS TO; INOUE- periods; lack of effective insecticides or practical at the present time. NAGATA AK. 2012b. Further characterization of tomato-infecting begomoviruses in Brazil. and emergence of insecticide-resistant It is also imperative that efforts to Archives of Virology 157: 747-752. whitefly populations; and the widespread manage the whiteflies and begomovirus ARAGÃO FJ; NOQUEIRA ED; TINOCO ML; use of transgenic plants resistant to diseases are done on a regional basis. In FARIA JC. 2013. Molecular characterization worm pests (cotton, corn, and soybean) this regard, the capacity of all interested of the first commercial transgenic common bean immune to the Bean golden mosaic virus. that results in reduced application parties (academia, government, Journal of Biotechnology 166: 42-50. of broad-spectrum insecticides. This and growers) to get together and ARANHA SA; ALBUQUERQUE LC; BOITEUX means management of whiteflies and implement crop-free periods has been L; INOUE-NAGATA, AK. 2011.Detection the viruses they transmit will continue very encouraging. This will continue and complete genome characterization of a to be a major challenge for agriculture to require careful planning of such begomovirus infecting okra (Abelmoschus esculentus) in Brazil. Tropical Plant Pathology in Brazil and that the emergence of new periods, including the area and crops 36: 14-20. whitefly-transmitted virus diseases and to be included in different regions; BARBOSA JC; BARRETO SS; INOUE- changes in the biology of the whitefly the crop succession in each area; and NAGATA, AK; REZENDE JAM. 2011. should be expected. the development and implementation Characterization and experimental host range of a Brazilian tomato isolate of Tomato severe It should also be clear that management of an IPM strategy for each crop. rugose virus. Journal of Phytopathology 159: of whiteflies and begomovirus diseases Successful IPM packages will involve 644-646. cannot be accomplished by any single some combination of planting virus- BARBOSA LF; YUKI VA; MARUBAYASHI control measure, especially reliance on free propagative materials (e.g., sweet JM; MARCHI BR; PERINI FL; PAVAN MA; potato); utilizing resistant cultivars; BARROS DR; GHANIM M; MORIONES E; insecticides, and that an IPM approach NAVAS-CASTILLO J; KRAUSE-SAKATE is needed (Gilbertson et al., 2011). implementing effective whitefly R. 2015. 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