Cotton leaf curl Gezira virus
(African cotton leaf curl begomovirus)

Pictures

Picture	Title	Caption	Copyright
Title Field symptoms Caption Cotton leaf curl Gezira virus (African cotton leaf curl begomovirus); field symptoms, characteristic of CLCuGV in okra (Abelmoschus esculentus). Copyright ©Walter N. Leke/Institute of Agricultural Research for Development (IRAD), Cameroon.	Field symptoms	Cotton leaf curl Gezira virus (African cotton leaf curl begomovirus); field symptoms, characteristic of CLCuGV in okra (Abelmoschus esculentus).	©Walter N. Leke/Institute of Agricultural Research for Development (IRAD), Cameroon.
Title Field symptoms Caption Cotton leaf curl Gezira virus (African cotton leaf curl begomovirus); field symptoms, characteristic of CLCuGV in okra (Abelmoschus esculentus). Copyright ©Walter N. Leke/Institute of Agricultural Research for Development (IRAD), Cameroon.	Field symptoms	Cotton leaf curl Gezira virus (African cotton leaf curl begomovirus); field symptoms, characteristic of CLCuGV in okra (Abelmoschus esculentus).	©Walter N. Leke/Institute of Agricultural Research for Development (IRAD), Cameroon.
Title Field symptoms Caption Cotton leaf curl Gezira virus (African cotton leaf curl begomovirus); field symptoms, characteristic of CLCuGV in okra (Abelmoschus esculentus). Copyright ©Walter N. Leke/Institute of Agricultural Research for Development (IRAD), Cameroon.	Field symptoms	Cotton leaf curl Gezira virus (African cotton leaf curl begomovirus); field symptoms, characteristic of CLCuGV in okra (Abelmoschus esculentus).	©Walter N. Leke/Institute of Agricultural Research for Development (IRAD), Cameroon.
Title Field symptoms. Caption Cotton leaf curl Gezira virus (African cotton leaf curl begomovirus); field symptoms, characteristic of CLCuGV in okra (Abelmoschus esculentus). Copyright ©Walter N. Leke/Institute of Agricultural Research for Development (IRAD), Cameroon.	Field symptoms.	Cotton leaf curl Gezira virus (African cotton leaf curl begomovirus); field symptoms, characteristic of CLCuGV in okra (Abelmoschus esculentus).	©Walter N. Leke/Institute of Agricultural Research for Development (IRAD), Cameroon.

Identity

Preferred Scientific Name

• Cotton leaf curl Gezira virus

Preferred Common Name

• African cotton leaf curl begomovirus

Other Scientific Names

• Cotton leaf curl Gezira begomovirus

EPPO code

• CLCUGV

Summary of Invasiveness

Cotton leaf curl Gezira virus (CLCuGV) is endemic to the African Sahel region (Idris et al., 2000). It is an economically important cotton-infecting begomovirus, and poses a serious threat to cotton production. It causes yield loss in all affected cotton-growing areas in Africa. Losses are difficult to assess, but estimates range up to 20% when infection occurs early in the growing season and/or with highly susceptible cultivars.

Natural spread is mainly by the whitefly vector, Bemisia tabaci, which transmits the virus in a persistent, circulative manner. Viruliferous whiteflies on infested/infected plants harbouring CLCuGV imported to other countries are of concern for preventing introduction.

Taxonomic Tree

• Domain: Virus
•     Group: "ssDNA viruses"
•         Group: "DNA viruses"
•             Family: Geminiviridae
•                 Genus: Begomovirus
•                     Species: Cotton leaf curl Gezira virus

Notes on Taxonomy and Nomenclature

Leaf curl disease refers to the symptom phenotype; this name has been given to leaf curl diseases of cotton caused by a number of different begomoviral species. Leaf curl in Africa was first reported in Nigeria in 1912 (Farquharson, 1912), followed by Sudan (Golding, 1930) and Tanzania (Kirkpatrick, 1931). When leaf curl symptoms were first observed in Pakistan in the mid-1960s (Hussain and Ali, 1975) the name ‘cotton leaf curl’ disease was erroneously adopted there based on reports of similar symptoms observed in cotton in Africa. Much later when begomoviral aetiology was established and begomoviral genome sequences became available (late 1990s-2010) it became clear that the cotton-infecting begomovirus in Africa was a distinct species, diverging significantly from the leaf curl disease begomovirus complex in South Asia e.g. India and Pakistan.

The Cotton leaf curl Gezira virus (CLCuGV) (some isolates, misnamed as Okra enation leaf curl virus, OKEV) is recognized as a distinct species having its origin in the Sahel region and nearby locales in Africa. The genome was first sequenced from cotton plants collected in Wad Madani, the State of Gezira, located between the Blue and White Nile in east-central Sudan (Idris and Brown, 2002; AF155064). It is the only begomovirus species known to infect cotton.

Some of the closest relatives of CLCuGV are monopartite begomoviral species infecting malvaceous species such as hollyhock and okra in the Sahel. Examples are the Hollyhock leaf crumple/Hollyhock leaf curl viruses, and Okra leaf curl Cameroon virus (OLCuCMV), indicating CLCuGV and closest relatives share African endemism. This close relatedness is further illustrated by their common association with a cotton leaf curl Gezira betasatellite (CLCuGeB) (collectively, >93% nt identity), and two alphasatellites, cotton leaf curl Gezira alphasatellite (CLCuGeA) and okra leaf curl Burkina Faso alphasatellite (OLCuBFA), respectively, that share a collective 95-97% nt identity (Leke et al., 2013). This complex of begomoviruses therefore differs biologically from the Cotton leaf curl disease (CLCuD)- ‘core’ begomoviruses, endemic to South Asia, by lacking cotton as a common host plant species.

The CLCuGV species is classified in the genus, Begomovirus; family, Geminiviridae. It has a monopartite genome of ~2.8 kb in size and an associated betasatellite of about one-half unit size, or 1.4 kb. CLCuGV isolates typically have at least one associated betasatellite and alphasatellite molecule, respectively, each about one-half the size of the ‘helper’ virus genome, or 1.4 kb. They are classified in the genus, Betasatellite (family, Tolecusatellitidae), and in the geminialphaspecies, Colecusatellite, subfamily, Alphasatellitidae, respectively.

The CLCuGV-betasatellites depend entirely on their helper virus for replication, cell-to-cell and long-distance movement in plants, encapsidation, and whitefly vector mediated-transmission. For helper virus systemic infection, they are essential determinants of pathogenicity, being required for symptom development (see references in Zhou, 2013). Betasatellites are ‘promiscuous’ and can be trans-replicated in the presence of multiple helper begomoviruses. They are relatively, minimally divergent at the species level (genus-level species cut-off, 78%).

The CLCuGV-‘satellite-like’ molecules, referred to as alphasatellites (previously, DNA-1), which encode an RCR (alpha-Rep) initiator protein (as do begomoviruses), a rolling-circle replication initiator protein, making them capable of autonomous replication, though they rely on a helper virus for encapsidation and thus, for whitefly-mediated transmission. They can be more divergent than betasatellites, at 70% and 88% pairwise identity. Studies have shown that alphasatellites may influence symptom phenotype by modulating host plant, helper viral, or betasatellite gene function, however, in other examples such as the ‘symptomless’ alphasatellites their contribution to the infection cycle is unknown. Although poorly understood, evidence suggests that alphasatellites may contribute to host adaptation and fitness, albeit, they may vary among different plant host-helper begomovirus-betasatellite combinations.

Description

Characteristic geminate or paired icosahedral virus particles (20 x 30 nm) have been observed by electron microscopy from leaf curl begomovirus-infected plants. Complete genome sequences are available for multiple isolates of the leaf curl complex begomoviruses and their betasatellites and alphasatellites (see ICTV for current species list: https://talk.ictvonline.org/ictv-reports/ictv_online_report/ssdna-viruses/w/geminiviridae/392/genus-begomovirus (Fauquet et al., 2008; Brown et al., 2012; Brown et al., 2015).

Distribution

Leaf curl disease of cotton in Africa has been reported in all countries where studies could be conducted north of the equator (Golding 1930; Tarr, 1951; Nour and Nour, 1964; Cauquil and Follin, 1983; Brown, 1994) and most studies published between 1912 and the mid-1980s centred on leaf curl isolates from Nigeria and Sudan. The recent use of molecular virology tools to identify CLCuGV has confirmed the virus is widespread throughout the cotton belt in subSaharan Africa/Sahel region (see references in Tiendrébéogo et al., 2010; Leke et al., 2013; Leke et al., 2015) where it has been reported from symptomatic cotton, cucumber, hollyhock, okra, Sida spp., tomato and a number of wild hosts representing several plant families (Idris et al., 2002a, 2002b, 2013, 2014).

Molecular cloning and DNA sequencing has facilitated the identification and characterization of CLCuGV-satellite complexes in some of the locations where historically, leaf curl symptoms were observed in cotton. Although cotton is no longer produced in some of these countries/locations, the distribution of CLCuGeV (primarily in okra and vegetable crops and wild species, has been corroborated in Benin, Burkina Faso, Cameroon, Chad, Côte d'Ivoire, Egypt, Niger, Nigeria, Sudan, Togo and other African countries where cotton is grown and where it is thought to have originated, but now occurs in locales outside of Africa. Similar to scenarios involving the CLCuD-begomoviruses in South Asia, CLCuGV has been shown to infect a broad range of host plants, making it and the CLCuD-begomoviruses problematic in cotton-vegetable production systems often found in irrigated agriculture where cotton is grown.

Recently CLCuGV has been identified infecting okra and/or tomato plant hosts in the Arabian Peninsula including Oman, Saudi Arabia and United Arab Emirates (see references in Idris et al., 2014) but how widespread the virus is and whether the isolates represent endemic and/or introduced strains is not yet entirely certain. The genome sequences of CLCuGV isolates from Saudi Arabia proved to be divergent from the previously reported isolates from Sudan, at 88-93% shared nt identity, suggesting these isolates might be endemic or that they are introductions that have been present, but gone undetected for some time. The genome of the UAE isolate shared its highest nt identity (96 to 97%) with isolates from Egypt (AF155064), Pakistan (FR751142) and Jordan (GU945265). In contrast, the UAE isolate shared 93% identity with an isolate of CLCuGeV (HG530540) from the west coast of Saudi Arabia. The 1,356-bp betasatellite shared its highest nt identity, at 97%, with the Okra leaf curl Oman betasatellite (KF267444) reported from infected okra plants in a neighbouring country, Oman.

During 2005, a CLCuGV isolate sharing high nt sequence identity with CLCuGV from Egypt, was identified from symptomatic cotton from the Sindh Province southern Pakistan, providing robust evidence for a recent introduction from northern Africa (Tahir et al., 2011).

Apparently, the introduction occurred from North Africa to West Africa, and from the Middle East to South Asia. There is no evidence the virus has spread from where it is believed to have been introduced. The symptomatic plants infected by CLCuGV in Pakistan contained no detectable CLCuGB. Also, whitefly mitotypes from Africa likely required for CLCuGV transmission, are not known to occur in Pakistan, except for a B-like mitotype that is not widely distributed in cotton (Masood et al., 2017). The latter two factors may explain why the CLCuGV from Africa has not spread.

From the Middle East, CLCuGV was detected in DNA isolated from whiteflies sampled in Israel and Jordan during 2011. This discovery suggested the possible long-distance dispersal of the CLCuGV by whiteflies, or that it had been introduced some years earlier, and had not yet been detected in plants. Subsequently, CLCuGV was identified infecting tomato plants in Jordan (Anfoka et al., 2014) and Israel (Gelbart et al., 2020). Conduits for dispersal are thought to have occurred through the plant trade and/or by viruliferous whiteflies associated with the plant trade because the CLCuGV betasatellite (CLCuB) also occurs in the east coast of the Mediterranean Sea and Middle East. In Israel, CLCuB has been shown to transreplicate TYLCV-IL and TYLCV-Mld, species endemic to Israel and Jordan (Gelbart et al., 2020).

Most recently, during 2019, the complete monopartite genome sequence of the CLCuGV was determined from symptomatic okra plants in south Texas, USA. The genome (2,764 nt) and shared 99.5 to 99.6% nt identity with an isolate of CLCuGV from hollyhock plants in Jordan (CLCuGV-[JO:Hol:09]: GU945265). The closest relative of the CLCuGA okra isolate, of 1,354 nt (MN027203 to 05), was CLCuGA-[IL:IsSq-C171:11] (KT099176), an isolate sequenced from whiteflies collected from squash plants in Israel, at 99% identity. This strongly suggests the virus-betasatellite complex was introduced from the Middle East, perhaps through the transport of plants and/or viruliferous whiteflies associated with the plant trade.

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Introductions

Risk of Introduction

Viruliferous whiteflies on infested/infected plants harbouring CLCuGV imported to other countries are of concern for preventing introduction under optimal circumstances. No seed transmission is known to occur.

Habitat List

Hosts/Species Affected

Alternative hosts and their role in disease epidemiology are still poorly documented, and studies are needed to identify the most important reservoirs of CLCuD-begomoviruses that most directly affect cotton. Gossypium hirsutum and G. barbadense are the predominant economic species.

The natural host range of the leaf curl virus isolates studied from various locations on the African continent is more moderate than the CLCuD-begomovirus complex in South Asia, and includes a number of species within the Malvaceae and at least several other plant families. The natural and experimental host range of CLCuGV from Africa are reported to include Capsicum annuum, Cucumis pepo, Gossypium spp, Hibiscus spp., Lycopersicon esculentum, okra, papaya, and several species within the genera Althaea, Amaranthus and Asystasia. Among the wild hosts reported are: Corchorus fascicularis, Lavatera cretica, Malva spp., Malvaviscus arboreus, Pavonia hastata, Sida spp. and wild hollyhock (Anfoka GH, MF522207 GenBank database); (Tarr, 1951; Nour and Nour, 1964; Bink, 1975; Cauquil and Follin, 1983; Fauquet and Thouvenel, 1987; Brown, 1992; Gambley et al., 2020).

Host Plants and Other Plants Affected

Growth Stages

Symptoms

CLCuGV-infected cotton exhibits upward or downward leaf curling, accompanied by foliar discoloration and mosaic. In addition, leaves show minor- and major-vein thickening, a characteristic that may depend on the cotton variety. Cotton plants infected in early growth stages show shortened internodes and dramatic stunting. A less severe symptom phenotype referred to as small vein thickening, which is characterized by the development of minute foliar enations on the veins and a slight mosaic and leaf curling has been documented in Nigeria and Sudan (Idris, 1990; Brown, 1992; Brown, 1994).

List of Symptoms/Signs

Biology and Ecology

Cotton leaf curl Gezira virus is transmitted by the whitefly vector Bemisia tabaci cryptic species complex. Disease incidence is dependent on climatic factors that influence population levels of the whitefly vector. Periods of high rainfall prior to planting promotes the growth of weeds, which serve as hosts of the whitefly and as reservoirs of the virus. Cotton is the primary site of infection as the virus is transmitted by viruliferous whiteflies arising from infected weed hosts. Secondary spread occurs within infected cotton fields, and can be extremely rapid under moderate-to-high vector population levels. In Sudan, the greatest whitefly vector populations and the highest disease incidence has been reported to occur in October-November following August-September planting dates (Idris, 1990; Brown, 1992, 1994, 2002; Idris and Brown, 2002).

Whitefly vector transmission

Studies have shown that begomoviruses are transmitted by a number of phylogeographically-distributed cryptic species (and mitotypes, therein) of the whitefly vector B. tabaci (Brown, 2010; De Moya et al., 2019). In the Sahel region of Africa, the Q-type mitotypes are predominant in central and eastern Africa, while one or more B-types occur in Egypt and Arabia (Brown, 2010). Begomoviruses are transmitted in a persistent, circulative manner and once acquired, transmission can occur throughout the life of the vector. The virus is not transovarially transmitted.

Environmental factors such as the whitefly vector mitotype, itself differentially responsive to insecticides and prone to development of insecticide resistance, are thought to influence in part the fluctuations in virus composition from season to season. An exacerbating factor is that different mitotypes are known to exhibit differential transmission competency among members of the CLCuGV-begomovirus-satellite complexes (Bedford et al., 1994; Guo et al., 2015; Pan et al., 2018; Chen et al., 2019). Detailed studies of mitotype competency have not been carried out for the CLCuGV and its endemic whitefly vector mitotype(s).

Climate

Pathway Causes

Pathway Vectors

Plant Trade

Vectors and Intermediate Hosts

Impact Summary

Impact

Cotton leaf curl Gezira virus has been responsible for yield loss in all affected cotton-growing areas in Africa since its discovery. Losses are difficult to assess, but estimates range up to 20% when infection occurs early in the growing season and/or with highly susceptible cultivars. Losses are due to fewer bolls set and reduced boll weight (Andrews, 1936; Bedford, 1938; Bougher, 1947; Tarr, 1964; Ahmed, 1987). Most susceptible varieties in Sudan are GS(83)3, Domains Sakel and Bar 14/25; these varieties are no longer grown in areas where the disease is prevalent. The close proximity of okra to cotton fields has been directly associated with high leaf curl disease incidence in cotton (Idris, 1990), suggesting that okra may be an important reservoir of the virus for cotton crops. 

Risk and Impact Factors

• Invasive in its native range
• Proved invasive outside its native range
• Has a broad native range
• Abundant in its native range
• Reproduces asexually
• Has high genetic variability

• Host damage
• Negatively impacts agriculture
• Negatively impacts livelihoods
• Reduced native biodiversity
• Negatively impacts animal/plant collections
• Negatively impacts trade/international relations

• Competition (unspecified)
• Pest and disease transmission
• Hybridization
• Pathogenic

• Highly likely to be transported internationally accidentally
• Highly likely to be transported internationally deliberately
• Highly likely to be transported internationally illegally
• Difficult to identify/detect as a commodity contaminant
• Difficult to identify/detect in the field
• Difficult/costly to control

Diagnosis

Antisera raised to purified virions of a number of begomoviruses have been used for virus detection in symptomatic leaves. Serology has been useful for detection but not for species-level identification (Swanson et al., 1992; Swanson et al., 1993).

Begomoviruses can be detected by DNA-DNA hybridization with non-radioactively-labelled cloned begomoviral fragments from a panel of divergent species allowing for differential detection of a number of begomoviruses (Brown and Poulos, 1990; Brown and Poulos, 1991; Swanson et al., 1992).

Membrane-bound total DNA from leaf squashes onto FTA cards (Whatman International Ltd., Maidstone, UK) (Leke et al., 2007; Leke et al., 2013) has been used as template for PCR amplification using general begomovirus primers (Wyatt and Brown, 1996) and the viral genome and associated satellites can first be enriched using rolling circle amplification (RCA) (Inoue-Nagata et al., 2004).

Polymerase chain reaction (PCR) amplification of one of several conserved regions of the virus genome has been used to detect infection by CLCuD-begomoviruses and/or alphasatellites and/or betasatellites in cotton and other CLCuD-begomovirus plant hosts by a number of laboratories worldwide (Wyatt and Brown, 1996; Brown et al., 2001, 2017; Briddon et al., 2002; Bull et al., 2003; Radhakrishnan et al., 2004; Chakrabarty et al., 2005; Monga et al., 2005; Sharma et al., 2005; Kumar et al., 2018) and in whiteflies (Rosario et al., 2015; Rosario et al., 2016).

Amplification by PCR and cloning followed by primer walking, or by high-throughput DNA sequencing of viral genome and betasatellite components are used to detect and identify begomovirus isolates, strains and species (Idris et al., 2014). Validation of PCR amplicons from suspect-begomovirus infected plants is accomplished by cloning and sequencing, and comparative sequence analysis, initially by a BLASTn search of the NIH-NCBI GenBank database. Greater scrutiny is applied by alignment of selected sequences of interest, and pairwise distance analysis using the RDP algorithm (Muhire et al., 2013). Species demarcation criteria available at the ICTV website and other published references (see Taxonomy and Nomenclature).

Whitefly vector-mediated transmission from symptomatic plant samples suspected to be infected by CLCuD begomoviruses to cotton indicator plants is a reliable bioassay method when a virus-free, whitefly vector colony is available.

Detection and Inspection

Leaf curling, vein-thickening, and minor veinal enations on undersides of leaves are common symptoms of Cotton leaf curl Gezira virus. Leaf curling, distortion and shortened internodes, with symptoms occurring particularly on the newest growth, are diagnostic for begomovirus-incited diseases. Foliar discoloration, sometimes bright or dull yellow and/or green mosaic and mottling, are symptoms accompanying foliar curling, particularly on the newest growth, are diagnostic for begomovirus infection.

Similarities to Other Species/Conditions

The leaf curl viruses of cotton are most closely related to other begomoviruses (Geminiviridae), based on particle morphology, genome sequence and organization, and transmission by a whitefly vector, Bemisia tabaci.

Prevention and Control

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Resistant varieties XL1, L1530, X1730A, X1030 and B6L were developed for cotton growing areas in the African Sahel and adjacent locales through selection in the 1930s. These exhibit a mild mosaic but produce viable yields and high quality, marketable cotton. The mechanism of resistance was thought to involve reduction in virus levels in infected plants, and these lines have apparently proven durable.

Chemical control to reduce whitefly vector populations, and hence virus inoculum levels, is effective when population pressures are low; but recent upsurges in vector populations due to changing agricultural practices and development of insecticide resistance have made this a less than satisfactory solution (Sippell et al., 1987). No recent reports of new cotton varieties released for Africa could be located. One report indicated Sudan was experiencing a crisis in insect control in cotton (Eveleens, 1983) and another promoted the use of natural enemies for whitefly control in the Gezira (Abdelrahman, 1986). Elimination of weeds near cotton fields may have some advantage in reducing virus and vector reservoirs. Host-plant resistance is undoubtedly the most promising means of controlling this disease and renewed efforts are under way in several laboratories around the world to work toward this goal.

References

Abdelrahman, A. A., 1986. The potential of natural enemies of the cotton whitefly in Sudan Gezira. Insect Science and its Application, 7(1), 69-73.

Ahmed KE, 1987. MSc thesis: Field evaluation of selected strains of cotton, Gossypium barbadense L. for resistance to leaf curl virus disease and its effect on cotton yield and quality. Sudan: University of Gezira.

Akhtar, S., Khan, A. J., Singh, A. S., Briddon, R. W., 2014. Identification of a disease complex involving a novel monopartite Begomovirus with beta- and alphasatellites associated with okra leaf curl disease in Oman. Archives of Virology, 159(5), 1199-1205. doi: 10.1007/s00705-013-1926-x

Andrews, F. W. , 1936. The effect of leaf curl disease on the yield of the Cotton plant. Empire Cotton Growing Review, 13(4), 287-293 pp.

Anfoka, G., Ahmad, F. H., Altaleb, M., Abadi, M., 2014. Detection of satellite DNA beta in tomato plants with tomato yellow leaf curl disease in Jordan. Plant Disease, 98(7), 1017. http://apsjournals.apsnet.org/loi/pdis

Bedford, H. W., 1938. Agricultural Research Service, Anglo Egyptian Sudan, 1937. 50-65.

Bedford, I. D., Briddon, R. W., Brown, J. K., Rosell, R. C., Markham, P. G., 1994. Geminivirus transmission and biological characterisation of Bemisia tabaci (Gennadius) biotypes from different geographic regions. Annals of Applied Biology, 125(2), 311-325. doi: 10.1111/j.1744-7348.1994.tb04972.x

Bink, F. A., 1975. Leafcurl and mosaic diseases of cotton in central Africa. Cotton Growing Review, 52(3), 233-241.

Bougher, A. S., 1947. The causes of variation in the incidence of cotton leaf curl in the Sudan Gezira. In: Imperial Mycological Institute Mycological Paper , 22. 1-9.

Briddon RW, Bull SE, Mansoor S, Amin I, Markham PG, 2002. Universal primers for the PCR-mediated amplification of DNA beta: a molecule associated with some monopartite begomoviruses. Molecular Biotechnology, 20(3), 315-318.

Briddon, R. W., Brown, J. K., Moriones, E., Stanley, J., Zerbini, M., Zhou, X., Fauquet, C. M., 2008. Recommendations for the classification and nomenclature of the DNA-β satellites of begomoviruses. Archives of Virology, 153(4), 763-781. doi: 10.1007/s00705-007-0013-6

Briddon, R. W., Martin, D. P., Roumagnac, P., Navas-Castillo, J., Fiallo-Olivé, E., Moriones, E., Lett, J. M., Zerbini, F. M., Varsani, A., 2018. Alphasatellitidae: a new family with two subfamilies for the classification of geminivirus- and nanovirus-associated alphasatellites. Archives of Virology, 163(9), 2587-2600. doi: 10.1007/s00705-018-3854-2

Brown JK, 2010. Bemisia: Phylogenetic biology of the Bemisia tabaci sibling species group. In: Bemisia: Bionomics and Management of a Global Pest, Netherlands: Springer. 31-67.

Brown JK, Fauquet CM, Briddon RW, Zerbini M, Moriones E, Navas-Castillo J, 2012. Geminiviridae. In: Virus taxonomy: classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses, [ed. by King AMQ, Lefkowitz EJ, Adams MJ, Carstens EB]. San Diego, USA: Elsevier Academic Press. 351-373.

Brown JK, Poulos BT, 1990. Semi-quantitative DNA hybridization analysis of whitefly-transmitted geminiviruses. Phytopathology, 80, 888.

Brown JK, Poulos BT, Bird J, 1992. Differential detection of whitefly-transmitted geminiviruses in weed species from Puerto Rico by hybridization analysis with non-radioactive probes. In: APS-Caribbean Div. Meetings, Mayaguez, PR, May 1991

Brown, J. K., 1992. Virus diseases. In: Cotton diseases [ed. by Hillocks, R.J.]. Wallingford, UK: CAB International.275-329.

Brown, J. K., 1994. Current status of Bemisia tabaci as a plant pest and virus vector in agroecosystems worldwide. FAO Plant Protection Bulletin, 42(1/2), 3-32.

Brown, J. K., Frohlich, D. R., Rosell, R. C., 1995. The sweetpotato or silverleaf whiteflies: biotypes of Bemisia tabaci or a species complex?. Annual Review of Entomology, 40, 511-534. doi: 10.1146/annurev.en.40.010195.002455

Brown, J. K., Idris, A. M., Torres-Jerez, I., Banks, G. K., Wyatt, S. D., 2001. The core region of the coat protein gene is highly useful for establishing the provisional identification and classification of begomoviruses. Archives of Virology, 146(8), 1581-1598. doi: 10.1007/s007050170080

Brown, J. K., Zerbini, F. M., Navas-Castillo, J., Moriones, E., Ramos Sobrinho, R., Silva, J. C. F., Fiallo-Olivé, E., Briddon, R. W., Hernández-Zepeda, C., Ali Idris, Malathi, V. G., Martin, D. P., Rivera-Bustamante, R., Ueda, S., Varsani, A., 2015. Revision of Begomovirus taxonomy based on pairwise sequence comparisons. Archives of Virology, 160(6), 1593-1619. doi: 10.1007/s00705-015-2398-y

Brown, J. K., Zia-Ur-Rehman, M., Avelar, S., Chingandu, N., Hameed, U., Haider, S., Ilyas, M., 2017. Molecular diagnostic development for begomovirus-betasatellite complexes undergoing diversification: a case study. Virus Research, 241, 29-41. doi: 10.1016/j.virusres.2017.04.014

Bull S, Briddon RW, Markham P, 2003. Universal primers for the PCR-mediated amplification of DNA1: A satellite-like molecule associated with begomovirus-DNA β complexes. Molecular Biotechnology, 23, 83-86.

Cauquil, J., Follin, J. C., 1983. Presumed virus and mycoplasma-like organism diseases in subsaharan Africa and in the rest of the world. (Les maladies du cotonnier attribuees a des virus ou a des mycoplasmes en Afrique au Sud du Sahara et dans le reste du Monde). Coton et Fibres Tropicales, 38(4), 293-317.

Chakrabarty, P. K., Sable, S., Monga, D., Mayee, C. D., 2005. Polymerase chain reaction-based detection of Xanthomonas axonopodis pv. malvacearum and cotton leaf curl virus. Indian Journal of Agricultural Sciences, 75(8), 524-528.

Chen T, Saeed Q, He Z, Lu L, 2019. Transmission efficiency of Cotton leaf curl Multan virus by three cryptic species of Bemisia tabaci complex in cotton cultivars. PeerJ, 7, e7788.

De Moya RS, Brown JK, Sweet AD, Walden KKO, Paredes Montero JR, Waterhouse RM, Johnson KP, 2019. Nuclear orthologs derived from whole genome sequencing indicate cryptic diversity in the Bemisia tabaci (Insecta: Aleyrodidae) complex of whiteflies. Diversity, 11, 151.

Eveleens, K. G., 1983. Cotton-insect control in the Sudan Gezira: analysis of a crisis. Crop Protection, 2(3), 273-287. doi: 10.1016/0261-2194(83)90002-9

Farquharson, C. O., 1912. Annual Report, Agricultural Department, Nigeria. Nigeria: Agricultural Department

Fauquet, C, Thouvenel, JC, 1987. Plant Viral Disease in the Ivory Coast. Paris, Editions de L'ORSTOM, Institut Francais de Recherche Scientifique pour le Developpement en Cooperation.

Fauquet, C. M., Briddon, R. W., Brown, J. K., Moriones, E., Stanley, J., Zerbini, M., Zhou, X., 2008. Geminivirus strain demarcation and nomenclature. Archives of Virology, 153(4), 783-821. doi: 10.1007/s00705-008-0037-6

Gambley, C., Cremer, J., Campbell, P., Roach, R., Abdel-Salam, A. M., 2020. New host records for Cotton leaf curl Gezira virus: capsicum and melon in Egypt. Australasian Plant Disease Notes, 15(3), (03 January 2020). doi: 10.1007/s13314-019-0372-3

Gelbart, D., Chen, L., Alon, T., Dobrinin, S., Levin, I., Lapidot, M., 2020. The recent association of a DNA betasatellite with Tomato yellow leaf curl virus in Israel - a new threat to tomato production. Crop Protection, 128, 104995. doi: 10.1016/j.cropro.2019.104995

Golding, F. D., 1930. A vector of leaf curl of Cotton in Southern Nigeria. Empire Cotton Growing Review, 7(2), 120-126 pp.

Guo Tao, Guo Qi, Cui XiYun, Liu YinQuan, Hu Jian, Liu ShuSheng, 2015. Comparison of transmission of Papaya leaf curl China virus among four cryptic species of the whitefly Bemisia tabaci complex. Scientific Reports, 5(1), 15432. http://www.nature.com/articles/srep15432

Hussain T, Ali M, 1975. A review of cotton diseases in Pakistan. Pak. Cottons, 19, 71-86.

Idris, A. M., 1990. Cotton leaf curl virus disease in the Sudan. In: Mededelingen van de Faculteit Landbouwwetenschappen, Rijksuniversiteit Gent , 55(2a) . 263-267.

Idris, A. M., Brown, J. K., 2000. Identification of a new, monopartite begomovirus associated with leaf curl disease of cotton in Gezira, Sudan. Plant Disease, 84(7), 809. doi: 10.1094/PDIS.2000.84.7.809C

Idris, A. M., Brown, J. K., 2002. Molecular analysis of Cotton leaf curl virus-Sudan reveals an evolutionary history of recombination. Virus Genes, 24(3), 249-256. doi: 10.1023/A:1015380600089

Idris, A. M., Brown, J. K., 2005. Evidence for interspecific-recombination for three monopartite begomoviral genomes associated with the tomato leaf curl disease from central Sudan. Archives of Virology, 150(5), 1003-1012. doi: 10.1007/s00705-004-0484-7

Idris, A. M., Shahid, M. S., Briddon, R. W., Khan, A. J., Zhu, J. K., Brown, J. K., 2011. An unusual alphasatellite associated with monopartite begomoviruses attenuates symptoms and reduces betasatellite accumulation. Journal of General Virology, 92(3), 706-717. doi: 10.1099/vir.0.025288-0

Idris, A. M., Smith, S. E., Brown, J. K., 2001. Ingestion, transmission, and persistence of Chino del tomate virus (CdTV), a New World begomovirus, by Old and New World biotypes of the whitefly vector Bemisia tabaci. Annals of Applied Biology, 139(1), 145-154. doi: 10.1111/j.1744-7348.2001.tb00139.x

Idris, A., Al-Saleh, M., Amer, M., Abdalla, O., Brown, J., 2014. Introduction of Cotton leaf curl Gezira virus into the United Arab Emirates. Plant Disease, 98(11), 1593. doi: 10.1094/PDIS-08-14-0838-PDN

Inoue-Nagata, A. K., Albuquerque, L. C., Rocha, W. B., Nagata, T., 2004. A simple method for cloning the complete begomovirus genome using the bacteriophage φ29 DNA polymerase. Journal of Virological Methods, 116(2), 209-211. doi: 10.1016/j.jviromet.2003.11.015

Jiu, M., Zhou, X. P., Liu, S. S., 2006. Acquisition and transmission of two begomoviruses by the B and a non-B biotype of Bemisia tabaci from Zhejiang, China. Journal of Phytopathology, 154(10), 587-591. doi: 10.1111/j.1439-0434.2006.01151.x

Khan, A. J., Akhtar, S., Al-Shihi, A. A., Al-Hinai, F. M., Briddon, R. W., 2012. Identification of Cotton leaf curl Gezira virus in papaya in Oman. Plant Disease, 96(11), 1704. doi: 10.1094/PDIS-05-12-0438-PDN

Kirkpatrick, T. W., 1931. Further studies on leaf curl of cotton in the Sudan. Bulletin of Entomological Research, 12, 323-363.

Konaté, G., Barro, N., Fargette, D., Swanson, M. M., Harrison, B. D., 1995. Occurrence of whitefly-transmitted geminiviruses in crops in Burkina Faso, and their serological detection and differentiation. Annals of Applied Biology, 126(1), 121-129. doi: 10.1111/j.1744-7348.1995.tb05008.x

Leke W, Mignouna DB, Brown JK, Kvarnheden A, 2015. Begomovirus disease complex: Emerging virus diseases treat in vegetable production systems of West and Central Africa - A review. Agric. & Food Security, 4(1), http://dx.doi.org/10.1186/s40066-014-0020-2

Leke, W. N., Kvarnheden, A., Avelar, S., Brown, J. K., 2020. Molecular characterization of two previously undescribed begomovirus-associated alphasatellite molecules infecting malvaceous species in Cameroon. Archives of Virology, 165(3), 775-779. doi: 10.1007/s00705-020-04523-8

Leke, W. N., Ramsell, J. N. E., Njualem, D. K., Titanji, V. P. K., Legg, J. P., Fondong, V. N., Brown, J. K., Kvarnheden, A., 2007. FTA technology facilitates detection and identification of begomoviruses from okra plants in Cameroon. In: 8th African Crop Science Society Conference, El-Minia, Egypt, 27-31 October 2007 [8th African Crop Science Society Conference, El-Minia, Egypt, 27-31 October 2007], [ed. by Ahmed, K. Z.]. El-Minia, Egypt: African Crop Science Society. 655-660.

Leke, W. N., Sattar, M. N., Ngane, E. B., Ngeve, J. M., Kvarnheden, A., Brown, J. K., 2013. Molecular characterization of begomoviruses and DNA satellites associated with okra leaf curl disease in Cameroon. Virus Research, 174(1/2), 116-125. doi: 10.1016/j.virusres.2013.03.010

Mariyam Masood, Imran Amin, Ishtiaq Hassan, Shahid Mansoor, Brown, J. K., Briddon, R. W., 2017. Diversity and distribution of cryptic species of the Bemisia tabaci (Hemiptera: Aleyrodidae) complex in Pakistan. Journal of Economic Entomology, 110(6), 2295-2300. doi: 10.1093/jee/tox221

Monga D, Kumar R, Kumar M, 2005. Detection of DNA-A and satellite (DNA-ß) in cotton leaf curl virus (CLCuV) infected weeds and cotton plants using PCR technique. Journal of Cotton Research and Development, 19(1), 105-108.

Muhire, B., Martin, D. P., Brown, J. K., Navas-Castillo, J., Moriones, E., Zerbini, F. M., Rivera-Bustamante, R., Malathi, V. G., Briddon, R. W., Varsani, A., 2013. A genome-wide pairwise-identity-based proposal for the classification of viruses in the genus Mastrevirus (family Geminiviridae). Archives of Virology, 158(6), 1411-1424. doi: 10.1007/s00705-012-1601-7

Nour, M. A., Nour, Jane J., 1964. Identification, transmission, and host range of leaf curl viruses infecting Cotton in the Sudan. Empire Cotton Growing Review, 41(1), 27-37.

Pan LiLong, Cui XiYun, Chen QunFang, Wang XiaoWei, Liu ShuSheng, 2018. Cotton leaf curl disease: which whitefly is the vector?. Phytopathology, 108(10), 1172-1183. doi: 10.1094/phyto-01-18-0015-r

Paredes-Montero, J. R., Usman Hameed, Muhammad Zia-ur-Rehman, Ghulam Rasool, Haider, M. S., Herrmann, H. W., Brown, J. K., 2019. Demographic expansion of the predominant Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) mitotypes associated with the cotton leaf curl virus epidemic in Pakistan. Annals of the Entomological Society of America, 112(3), 265-280. doi: 10.1093/aesa/saz002

Pradeep Sharma, Narayan Rishi, Malathi, V. G., 2005. Molecular cloning of coat protein gene of an Indian cotton leaf curl virus (CLCuV-HS2) isolate and its phylogenetic relationship with others members of Geminiviridae. Virus Genes, 30(1), 85-91. doi: 10.1007/s11262-004-4585-x

Radhakrishnan, G., Malathi, V. G., Varma, A., 2004. Detection of DNA A and DNA β associated with cotton leaf curl and some other plant diseases caused by whitefly transmitted geminiviruses. Indian Phytopathology, 57(1), 53-60.

Rakesh Kumar, Palicherla, S. R., Bikash Mandal, Sreenu Kadiri, 2018. PCR based detection of betasatellite associated with the begomoviruses using improved universal primers. Australasian Plant Pathology, 47(1), 115-118. doi: 10.1007/s13313-017-0537-5

Rosario, K., Marr, C., Varsani, A., Kraberger, S., Stainton, D., Moriones, E., Polston, J. E., Breitbart, M., 2016. Begomovirus-associated satellite DNA diversity captured through vector-enabled metagenomic (VEM) surveys using whiteflies (Aleyrodidae). Viruses, 8(2), 36. doi: 10.3390/v8020036

Rosario, K., Seah YeeMey, Marr, C., Varsani, A., Kraberger, S., Stainton, D., Moriones, E., Polston, J. E., Duffy, S., Breitbart, M., 2015. Vector-enabled metagenomic (VEM) surveys using whiteflies (Aleyrodidae) reveal novel Begomovirus species in the new and old worlds. Viruses, 7(10), 5553-5570. doi: 10.3390/v7102895

Shih, S. L., Kumar, S., Tsai, W. S., Lee, L. M., Green, S. K., 2009. Complete nucleotide sequences of okra isolates of Cotton leaf curl Gezira virus and their associated DNA-β from Niger. Archives of Virology, 154(2), 369-372. doi: 10.1007/s00705-008-0304-6

Singh, J., Sohi, A. S., Mann, H. S., Kapur, S. P., 1994. Studies on whitefly, Bemisia tabaci (Genn.) transmitted cotton leaf curl disease in Punjab. Journal of Insect Science, 7(2), 194-198.

Sippell, D. W., Bindra, O. S., Khalifa, H., 1987. Resistance to whitefly (Bemisia tabaci) in cotton (Gossypium hirsutum) in the Sudan. Crop Protection, 6(3), 171-178. doi: 10.1016/0261-2194(87)90007-X

Swanson, M. M., Brown, J. K., Poulos, B. T., Harrison, B. D., 1992. Genome affinities and epitope profiles of whitefly-transmitted geminiviruses from the Americas. Annals of Applied Biology, 121(2), 285-296. doi: 10.1111/j.1744-7348.1992.tb03441.x

Swanson, M. M., Harrison, B. D., 1993. Serological relationships and epitope profiles of isolates of okra leaf curl geminivirus from Africa and the Middle East. Biochimie, 75(8), 707-711. doi: 10.1016/0300-9084(93)90101-W

Tahir, MN, Amin, I, Briddon, RW, Mansoor, S, 2011. The merging of two dynasties-identification of an African cotton leaf curl disease-associated begomovirus with cotton in Pakistan. PLoS ONE, 6(5), e20366. doi:10.1371/.

Tarr, S. A. J. , 1951. Leaf curl disease of cotton, Commonwealth Mycological Institute, Kew, Surrey.viii + 55 pp.

Tarr, S. A. J., 1964. Virus diseases of Cotton. Misc. Publs Commons. mycol. Inst, 18, 23 pp.

Tiendrébéogo, F., Lefeuvre, P., Hoareau, M., Villemot, J., Konaté, G., Traoré, A. S., Barro, N., Traoré, V. S., Reynaud, B., Traoré, O., Lett, J. M., 2010. Molecular diversity of Cotton leaf curl Gezira virus isolates and their satellite DNAs associated with okra leaf curl disease in Burkina Faso. Virology Journal, 7(48), (23 February 2010). http://www.virologyj.com/content/7/1/48

Villegas, C, Ramos Sobrinho, R, Jifon, JL, Keith, CV, Rwahnih, MH, Sétamou, M, Brown, JK, Alabi, OJ, 2019. First report of Cotton leaf curl Gezira virus and its associated alphasatellite and betasatellite from disease affected okra plants in the United States. Plant Disease, 103(12), 3291. https://doi.org/10.1094/PDIS-06-19-1175-PDN

Wyatt, S. D., Brown, J. K., 1996. Detection of subgroup III geminivirus isolates in leaf extracts by degenerate primers and polymerase chain reaction. Phytopathology, 86(12), 1288-1293. doi: 10.1094/Phyto-86-1288

Zhou XuePing, 2013. Advances in understanding begomovirus satellites. Annual Review of Phytopathology, 51, 357-381. doi: 10.1146/annurev-phyto-082712-102234

Distribution References

Abdel-Salam AM, 1999. Isolation and characterisation of a whitefly-transmitted geminivirus associated with the leaf curl and mosaic symptoms on cotton in Egypt. Arab J. Biotechnol. 193-218.

Al-Saleh M, Brown JK, Idris AM, 2014. Deep sequencing reveals Cotton leaf curl Gezira helper virus and sub-viral DNAs in weed, ornamental, and cultivated crops throughout Arabia. In: APS-CPS Joint Meeting, Minneapolis, MN. August 9-13, 2014, USA, APS-CPS.

Brown J K, 1992. Virus diseases. In: Cotton diseases. [ed. by Hillocks RJ]. Wallingford, UK: CAB International. 275-329.

CABI, 2020. CABI Distribution Database: Status as determined by CABI editor. Wallingford, UK: CABI

Cauquil J, Follin J C, 1983. Presumed virus and mycoplasma-like organism diseases in subsaharan Africa and in the rest of the world. (Les maladies du cotonnier attribuees a des virus ou a des mycoplasmes en Afrique au Sud du Sahara et dans le reste du Monde.). Coton et Fibres Tropicales. 38 (4), 293-317.

EPPO, 2020. EPPO Global database. In: EPPO Global database, Paris, France: EPPO.

Farquharson C O, 1912. Annual Report, Agricultural Department, Nigeria. Nigeria: Agricultural Department.

Fauquet C, Thouvenel JC, 1987. Plant Viral Disease in the Ivory Coast., Paris, Editions de L'ORSTOM, Institut Francais de Recherche Scientifique pour le Developpement en Cooperation.

Gambley C, Cremer J, Campbell P, Roach R, Abdel-Salam A M, 2020. New host records for Cotton leaf curl Gezira virus: capsicum and melon in Egypt. Australasian Plant Disease Notes. 15 (3), (03 January 2020). DOI:10.1007/s13314-019-0372-3

Golding F D, 1930. A vector of leaf curl of Cotton in Southern Nigeria. Empire Cotton Growing Review. 7 (2), 120-126 pp.

Idris A M, Brown J K, 2000. Identification of a new, monopartite begomovirus associated with leaf curl disease of cotton in Gezira, Sudan. Plant Disease. 84 (7), 809. DOI:10.1094/PDIS.2000.84.7.809C

Idris A M, Brown J K, 2002. Molecular analysis of Cotton leaf curl virus-Sudan reveals an evolutionary history of recombination. Virus Genes. 24 (3), 249-256. DOI:10.1023/A:1015380600089

Idris A M, Brown J K, 2005. Evidence for interspecific-recombination for three monopartite begomoviral genomes associated with the tomato leaf curl disease from central Sudan. Archives of Virology. 150 (5), 1003-1012. http://springerlink.metapress.com/link.asp?id=100423 DOI:10.1007/s00705-004-0484-7

Idris A, Al-Saleh M, Amer M, Abdalla O, Brown J, 2014. Introduction of Cotton leaf curl Gezira virus into the United Arab Emirates. Plant Disease. 98 (11), 1593. DOI:10.1094/PDIS-08-14-0838-PDN

Jones G H , Mason T G, 1926. On two obscure diseases of Cotton. Annals of Botany. 40 (160), 759-772 pp.

Khan A J, Akhtar S, Al-Shihi A A, Al-Hinai F M, Briddon R W, 2012. Identification of Cotton leaf curl Gezira virus in papaya in Oman. Plant Disease. 96 (11), 1704. DOI:10.1094/PDIS-05-12-0438-PDN

Kirkpatrick T W, 1931. Further studies on leaf curl of cotton in the Sudan. Bulletin of Entomological Research. 323-363.

Kirkpatrick T W, 1931a. Further studies on leaf-curl of Cotton in the Sudan. Bulletin of Entomological Research. 22 (3), 323-363 pp. DOI:10.1017/S0007485300029862

Shih S L, Kumar S, Tsai W S, Lee L M, Green S K, 2009. Complete nucleotide sequences of okra isolates of Cotton leaf curl Gezira virus and their associated DNA-ß from Niger. Archives of Virology. 154 (2), 369-372. DOI:10.1007/s00705-008-0304-6

Tahir MN, Amin I, Briddon RW, Mansoor S, 2011. The merging of two dynasties-identification of an African cotton leaf curl disease-associated begomovirus with cotton in Pakistan. PLoS ONE. 6 (5), e20366. doi:10.1371/.

Tiendrébéogo F, Lefeuvre P, Hoareau M, Villemot J, Konaté G, Traoré A S, Barro N, Traoré V S, Reynaud B, Traoré O, Lett J M, 2010. Molecular diversity of Cotton leaf curl Gezira virus isolates and their satellite DNAs associated with okra leaf curl disease in Burkina Faso. Virology Journal. 7 (48), (23 February 2010). http://www.virologyj.com/content/7/1/48

Villegas C, Ramos Sobrinho R, Jifon JL, Keith CV, Rwahnih MH, Sétamou M, Brown JK, Alabi OJ, 2019. First report of Cotton leaf curl Gezira virus and its associated alphasatellite and betasatellite from disease affected okra plants in the United States. Plant Disease. 103 (12), 3291. https://doi.org/10.1094/PDIS-06-19-1175-PDN

Contributors

01/06/20 Original text by:

Judith K Brown, School of Plant Sciences, The University of Arizona, Tucson, AZ 85721 USA

Distribution Maps