Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

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Cotton leaf curl disease complex
(leaf curl disease of cotton)

Brown J K, 2020. Cotton leaf curl disease complex (leaf curl disease of cotton). Invasive Species Compendium. Wallingford, UK: CABI. DOI:10.1079/ISC.16813.20210200739

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Cotton leaf curl disease complex (leaf curl disease of cotton)

Summary

  • Last modified
  • 10 December 2020
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Natural Enemy
  • Preferred Scientific Name
  • Cotton leaf curl disease complex
  • Preferred Common Name
  • leaf curl disease of cotton
  • Taxonomic Tree
  • Domain: Virus
  •   Group: "ssDNA viruses"
  •     Group: "DNA viruses"
  •       Family: Geminiviridae
  •         Genus: Begomovirus
  • Summary of Invasiveness
  • Leaf curl disease of cotton caused by the CLCuD-complex of begomoviruses is endemic to Pakistan and India and perhaps other nearby locales in south Asia. It has been introduced from there to China and the Philippines on ornamental plants, from whe...

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Pictures

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PictureTitleCaptionCopyright
Cotton leaf curl - minor vein thickening.
TitleSymptoms
CaptionCotton leaf curl - minor vein thickening.
Copyright©A.M. Idris
Cotton leaf curl - minor vein thickening.
SymptomsCotton leaf curl - minor vein thickening.©A.M. Idris

Identity

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Preferred Scientific Name

  • Cotton leaf curl disease complex

Preferred Common Name

  • leaf curl disease of cotton

Other Scientific Names

  • Cotton leaf curl Alabad virus
  • Cotton leaf curl Bangalore virus
  • cotton leaf curl bigeminivirus
  • cotton leaf curl geminivirus
  • Cotton leaf curl Kokhran virus- Kokhran
  • Cotton leaf curl Kokhran virus-Burewala
  • Cotton leaf curl Multan virus- Rajasthan
  • Cotton leaf curl Multan virus-Faisalabad strain

International Common Names

  • English: cotton leaf crinkle; cotton leaf curl disease; leaf crinkle of cotton
  • Spanish: hojas rizadas del algodonero
  • French: frisolée du cotonnier

  • CLCuMuV-Raj

English acronym

  • CLCuAlV
  • CLCuBaV
  • CLCuD complex
  • CLCuKoV-Bu
  • CLCuKoV-Ko
  • CLCuMuV-Fai
  • CLCuV

EPPO code

  • CLCuMuV (Cotton leaf curl Multan begomovirus) CLCuD ‘core’ complex

Summary of Invasiveness

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Leaf curl disease of cotton caused by the CLCuD-complex of begomoviruses is endemic to Pakistan and India and perhaps other nearby locales in south Asia. It has been introduced from there to China and the Philippines on ornamental plants, from where it has spread to infect cotton and okra in China. Losses are difficult to assess, but early estimates (pre-1990) range up to 20% when infection occurs early in the growing season and/or with highly susceptible cultivars

Viruliferous whiteflies on infested/infected plants harbouring CLCuD-begomoviruses imported to other cotton-growing countries, in particular, are of concern in preventing introduction under optimal circumstances. No seed transmission is known to occur.

Taxonomic Tree

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

Notes on Taxonomy and Nomenclature

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Leaf curl disease refers to the symptom phenotype; this name has been given to leaf curl diseases of cotton caused by different begomoviral species, Cotton leaf curl Alabad virus (CLCuAlV), Cotton leaf curl Bangalore virus (CLCuBaV), Cotton leaf curl Kokhran virus- Kokhran (CLCuKoV-Ko), Cotton leaf curl Kokhran virus-Burewala (CLCuKoV-Bu), Cotton leaf curl Multan virus (CLCuMuV) and Cotton leaf curl Multan virus-Rajasthan (CLCuMuV-Raj) that most commonly associate in cotton with one predominant betasatellite and alphasatellite and strains, thereof, respectively. Alphasatellites and betasatellites have no similarities to begomoviruses with respect to genome organization, however, they share in common a stem-loop structure and conserved origin of replication (TAATATTAC) that is required for initiation of rolling circle replication (RCR) by an RCR initiator protein.

Non-core begomoviruses identified in symptomatic cotton include: Cotton leaf curl virus-Lucknow (CLCuV-LKO-2), Okra enation leaf curl virus (OEnLCV), Papaya leaf curl virus (PaLCuV), Tomato leaf curl Bangalore virus (ToLCBaV) and Tomato leaf curl New Delhi virus (ToLCNDV) (Saeed, 2010; Sattar et al., 2013), pending further information about associated betasatellites/alphasatellites.

The leafhopper-transmitted geminiviruses, Chickpea chlorotic dwarf virus (CpCDV) (Mastrevirus: Geminiviridae) (also identified in tomato) (Zia-ur-Rehman et al., 2015) and the whitefly-transmitted bipartite Squash leaf curl virus, an exotic introduction from the Americas, are also recognized as non-core geminivirus contributors to the leaf curl disease of cotton in South Asia.

The core leaf curl begomoviruses of cotton fluctuate with respect to predominance in the various agroecosystems, shifting in response to genetically-different cotton varieties selected and released by breeding programmes, intended to abate leaf curl damage and outbreaks. Thus, at least five species and multiple variants (isolates) and strains are considered to have co-evolved in cotton in south Asia, and herein, are referred to as the ‘core’ species of the leaf curl disease complex, CLCuD. They are distinct species classified in the genus, Begomovirus; family, Geminiviridae. The viral genome is monopartite and ~2.8 kb in size (see references in Brown et al., 2017).

The core leaf curl begomoviruses have affiliated betasatellite of about one-half unit size of the ‘helper’ viral genome. 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 associated with CLCuD begomoviruses are ‘promiscuous’ in that they can be trans-replicated in the presence of multiple helper begomoviruses. For example, CLCuMuB has been reported to associate with at least six begomovirus species, either as single or multiple infections. They are relatively, minimally divergent at the species level (genus-level species cutoff, 78%). They are classified in the genus, Betasatellite (family, Tolecusatellitidae).

The most commonly associated betasatellites are strains of Cotton leaf curl Multan betasatellite (CLCuMuB), [CLCuMuBBur, CLCuMuBMul, CLCuMuBSha, CLCuMuBVeh], whereas, the most common alphasatellite-like component is Cotton leaf curl Multan alphasatellite (CLCuMuA). There are many other alphasatellites identified from various hosts, including cotton.

The CLCuD begomoviruses are also associated with ‘satellite-like’ molecules, referred to as alphasatellites (previously, DNA-1), which encode an RCR (alpha-Rep) initiator protein (as do begomoviruses), making them capable of autonomous replication. They are classified in the geminialphaspecies, Colecusatellite, subfamily, Alphasatellitidae.

The alphasatellite alpha-Rep is similar to the master Rep protein encoded by the genomic components (DNA-R) of nanoviruses and are classified as type I alphasatellites, distinguishing them from two other types, 2 and 3. The DNA1-type (previously, DNA-1 and DNA-2) is the most numerous, and they are the type associated with the CLCuD and other Old World begomoviruses. They require the helper begomovirus for in planta movement, encapsidation and whitefly-mediated transmission. Studies have shown that type I alphasatellites may influence symptom severity imparted by betasatellite βC1 that influences virulence by enhancing helper virus infectivity, possibly by reducing betasatellite accumulation (Idris et al., 2011). Some evidence suggests that alphasatellites may serve as determinants of host adaptation and fitness, however, their contributions appear to vary by plant host-helper begomovirus-betasatellite combination. 

Description

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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

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Leaf curl disease of cotton caused by the CLCuD-complex of begomoviruses is endemic to Pakistan and India and perhaps other nearby locales in south Asia. It has been introduced from there to China and the Philippines on ornamental plants, from where it has spread to infect cotton and okra in China.

Distribution Table

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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.

Last updated: 17 Feb 2021

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
China India 2006 Horticulture (pathway cause) Yes No Mao et al. (2008)
Philippines China 2012 Horticulture (pathway cause) No No Dolores et al. (2014)

Risk of Introduction

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Viruliferous whiteflies on infested/infected plants harbouring CLCuD-begomoviruses imported to other cotton-growing countries, in particular, are of concern in preventing introduction under optimal circumstances. No seed transmission is known to occur.

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial ManagedCultivated / agricultural land Present, no further details
Terrestrial ManagedProtected agriculture (e.g. glasshouse production) Present, no further details

Hosts/Species Affected

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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. Cotton, Gossypium hirsutum and G. barbadense, are the predominant economic species.

Growth Stages

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Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage

Symptoms

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Symptoms observed in cotton infected by the CLCuD-begomoviruses are upward or downward leaf curling, vein-thickening, and foliar discoloration. In addition, foliar enations of variable sizes are often observed growing from veins on the adaxial side of the leaf. When plants become infected in early growth stages, shortened internodes are commonly observed, and plants have a stunted appearance. Yield and quality of fibre are variably affected by leaf curl disease, depending on the cotton variety, begomovirus-satellite composition, including mixed infections and age of plant at time of infection (see references in: Brown, 1992; Brown, 1994; Brown, 2017; Mansoor et al., 2003).

List of Symptoms/Signs

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SignLife StagesType
Leaves / abnormal colours
Leaves / abnormal forms
Leaves / abnormal patterns
Whole plant / dwarfing

Biology and Ecology

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Attention was drawn to the disease in 1973 when leaf curl symptoms became prominent in the widely-grown cotton varieties, 149-F and B-557, in which symptoms were observed late in the growing season on flush growth, resulting in minimal damage (Hussain and Ali, 1975). By 1987, leaf curl incidence was as high as 80% in some cotton fields, damaging 60 ha in the Multan District. During 1991, leaf curl disease affected 14,000 ha in Multan, Khanewal, and Vehari Districts, and by 1992, 48,500 ha were infected. The heavy use of insecticides for whitefly control resulted in development of insecticide resistance, which led to unprecedented upsurges in whitefly vector populations. During the 1993 season the disease spread throughout the cotton belt of the Punjab Province, causing extensive yield loss in ~890,000 ha there, while also damaging hundreds of thousands of ha in the Indian Punjab. The virus was identified as CLCuMuV (Mansoor et al., 2003). Efforts during 1994-1997 to develop CLCuMuV-resistant cotton varieties were successful and cotton production returned to pre-epidemic levels.

During 2001-2002 a new leaf curl variant emerged, apparently originating in the Burewala territory, Punjab Province, that was able to infect cotton varieties developed with resistance to CLCuMuV, the causal agent of the 1994-1995 epidemic. Genome sequencing revealed the predominance of an emergent new species, initially, Cotton leaf curl-Burewala virus (CLCuBuV), but shortly, the name was changed to CLCuKoV-Bu, indicating a strain affiliation to CLCuKoV (Amrao et al., 2010). The viral genome was recombinant, consisting of sequence donated nearly equally from CLCuMuV and CLCuKoV (associated with the epidemic in the 1990s). Thus, from 2004-2007 until 2016-2017, CLCuKoV-Bu, a recombinant between CLCuKoV and CLCuMuV, referred to as ‘Burewala strain’ (AM421522) that became known as the ‘resistance-breaking’ strain became the most widespread. CLCuKoV-Bu and its betasatellite, CLCuMuBBur, spread throughout the cotton growing areas of Pakistan (Amin et al., 2006) and India (Rajagopalan et al., 2012). The virus was found to encode a truncated transactivator protein (TrAP) that was only 35 amino acids (aa) in size but was functionally active (Amrao et al., 2010; Kumar et al., 2015).

Cotton breeding lines shown to be resistant to CLCuKoV-Bur have subsequently found to be susceptible to CLCuKoV-Bur. Molecular analysis has confirmed the identity of the virus as CLCuKoV-Bur, however, it contained a longer version of the truncated TrAP gene, compared to that found for the original resistance-breaking strain, with a shorter form (Hassan et al., 2017), supporting the role of the truncated TrAP in resistance breaking, and illustrating the rapid restoration of a more virulent CLCuKoV-Bur isolate able to overcome recently selected resistant genetic materials. Isolates of CLCuMuV, CLCuKoV and CLCuAlV have full length TrAP coding regions and have been found infecting cotton, assisted by a new strain of CLCuMuB-Vehari strain (CLCuMuBVeh) (Zubair et al., 2017). Unexpectedly, surveys conducted after 2016 revealed the recurrence of a previously unreported CLCuMuV variant occurring widely in Pakistan and India (Datta et al., 2017; Zubair et al., 2017; Qadir et al., 2019; Ilyas et al., 2020) potentially negating the utility of cotton germplasm and improved varieties with apparent tolerance to CLCuKo-Bu selected prior to 2016.

CLCuMuV has been introduced into China as early as 2006 (Cai et al., 2010; Mao et al., 2008; Du et al., 2015) and the Philippines (Dolores et al., 2014) on infected malvaceous ornamental species.

CLCuGV has been detected in cotton plants in southern Pakistan during 2005, and the genomic sequence was most closely related to isolates from Egypt, suggesting a recent introduction (Tahir et al., 2011). The CLCuGB (betasatellite) was not detected in the infected plants. No further spread has been documented.

Whitefly vector transmission

Studies have shown that in South Asia, the CLCuD-begomoviruses are transmitted by several endemic cryptic species (and mitotypes, therein) (Bedford et al., 1994; Masood et al., 2017Paredes-Montero et al., 2019; Shah et al., 2020) of the whitefly vector Bemisia tabaci (Brown, 2010; De Moya et al., 2019; Paredes-Montero et al., 2019). The viruses 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.

Mixtures of begomovirus-betasatellites can occur in the same host plant and the CLCuD-begomovirus complex has been shown to be prone to rapid diversification, responding to changes in the cotton varieties developed to combat it. Thus, 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 CLCuD-begomovirus-satellite complexes (Jiu et al. 2006; Guo et al., 2015; Pan et al., 2018; Chen et al., 2019).

Also, ToLCNDV in mixed infection with CLCuKoV-Bu has been found to enhance the accumulation of CLCuMuBBur in the infected plants (Zaidi et al., 2015), which could favour CLCuD-begomovirus transmission from plants harbouring ToLCNDV plus CLCuD-viruses, over those that do not.

Disease incidence is dependent upon climatic factors that influence population levels of the whitefly vector. Periods of high rainfall prior to planting promote 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.

Climate

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ClimateStatusDescriptionRemark
As - Tropical savanna climate with dry summer Tolerated < 60mm precipitation driest month (in summer) and < (100 - [total annual precipitation{mm}/25])
Aw - Tropical wet and dry savanna climate Tolerated < 60mm precipitation driest month (in winter) and < (100 - [total annual precipitation{mm}/25])
B - Dry (arid and semi-arid) Tolerated < 860mm precipitation annually
BW - Desert climate Tolerated < 430mm annual precipitation
C - Temperate/Mesothermal climate Tolerated Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C
Cs - Warm temperate climate with dry summer Tolerated Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Cw - Warm temperate climate with dry winter Tolerated Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)

Pathway Causes

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Pathway Vectors

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Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Leaves Yes Pest or symptoms usually invisible
Seedlings/Micropropagated plants Yes Pest or symptoms usually invisible

Vectors and Intermediate Hosts

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VectorSourceReferenceGroupDistribution
Bemisia tabaciBrown et al. (1995); Brown (2010); De Moya et al. (2019)Insect

Impact Summary

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CategoryImpact
Economic/livelihood Negative

Impact

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Losses are difficult to assess, but early estimates (pre-1990) range up to 20% when infection occurs early in the growing season and/or with highly susceptible cultivars. Losses were due to fewer bolls set and reduced boll weight. In Pakistan, S-12 and CIM-70 developed severe disease symptoms of CLCuD, exhibiting dramatically shortened internodes, stunting and reduced fruit set and boll weight.

From 1990-onward, as much as 80% of plants in cotton fields in Pakistan and India have become infected early in the season and in some years entire plantings have been lost to the disease (Varma et al., 1993; Ajmera, 1994; Rishi and Chauhan, 1994; Mahmood et al., 2003; Buttar and Sekhon, 2017). 

Risk and Impact Factors

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Invasiveness
  • 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
Impact outcomes
  • Host damage
  • Negatively impacts agriculture
  • Negatively impacts livelihoods
  • Reduced native biodiversity
  • Negatively impacts animal/plant collections
  • Negatively impacts trade/international relations
Impact mechanisms
  • Competition (unspecified)
  • Pest and disease transmission
  • Hybridization
  • Pathogenic
Likelihood of entry/control
  • 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

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Antisera have been raised to purified virions of Cotton leaf curl virus or to other begomoviruses have been used for virus detection in symptomatic leaves (Swanson et al., 1992).

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; Briddon et al., 2002; Bull et al., 2003; Radhakrishnan et al., 2004; Chakrabarty et al., 2005; Monga et al., 2005; Sharma et al., 2005; Brown et al., 2017; 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 above).

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.

Nucleic acid spot hybridization (NASH) has been used by Radhakrishnan et al. (2004) to efficiently detect Cotton leaf curl virus in plants.

Detection and Inspection

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Leaf curling, vein-thickening, and veinal enations on undersides of leaves are common symptoms of CLCuD in South Asia. 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

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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

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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.

Chemical control to reduce whitefly vector populations, and hence virus inoculum levels, is effective when population pressures are low. Upsurges in vector populations due to changing agricultural practices and development of insecticide resistance have made this a less than satisfactory solution. Elimination of weeds near cotton fields may have some advantage in reducing virus and vector reservoirs. Host-plant resistance is the most desirable approach for controlling the cotton leaf curl disease and ongoing efforts are underway in India and Pakistan.

References

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Ahmed KE, 1987. 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. MSc. Thesis, University of Gezira

Ajmera, BD, 1994. Occurrence of leaf curl virus on American cotton (G. hirsutum) in north Rajasthan. In: National Seminar on Cotton Production Challenges in 21st Century, Hisar on April 18-20 . Hisar, Haryana, India: Choudhary Charan Singh Hisar Agricultural University.

Amin I, Mansoor S, Amrao L, et al., 2006. Mobilisation into cotton and spread of a recombinant cotton leaf curl disease satellite. Archives of Virology, 151, 2055–2065.

Andrews FW, 1936. The effect of leaf curl disease on the yield of the cotton plant. Empire Cotton Growers Review, 13:287-293

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

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 RW, Navas-Castillo J, Fiallo-Olivé E, et al., 2016. ICTV taxonomic proposal 2016.021a-kP.A.v2.Tolecusatellitidae. Create the Tolecusatellitidae, a new family of single-stranded DNA satellites with two genera. http://www.ictv.global/proposals-16/2016.021a-kP.A.v2.Tolecusatellitidae.pdf

Briddon, R. W., 2003. Cotton leaf curl disease, a multicomponent begomovirus complex. Molecular Plant Pathology, 4(6), 427-434. doi: 10.1046/j.1364-3703.2003.00188.x

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., Bull, S. E., Imran Amin, Idris, A. M., Shahid Mansoor, Bedford, I. D., Poonam Dhawan, Narayan Rishi, Siwatch, S. S., Abdel-Salam, A. M., Brown, J. K., Yusuf Zafar, Markham, P. G., 2003. Diversity of DNA β, a satellite molecule associated with some monopartite begomoviruses. Virology , 312(1), 106-121. doi: 10.1016/S0042-6822(03)00200-9

Briddon, R. W., Fazal Akbar, Zafar Iqbal, Luqman Amrao, Imran Amin, Muhammad Saeed, Shahid Mansoor, 2014. Effects of genetic changes to the Begomovirus/betasatellite complex causing cotton leaf curl disease in South Asia post-resistance breaking. Virus Research, 186, 114-119. doi: 10.1016/j.virusres.2013.12.008

Briddon, R. W., Mansoor, S., Bedford, I. D., Pinner, M. S., Saunders, K., Stanley, J., Zafar, Y., Malik, K. A., Markham, P. G., 2001. Identification of DNA components required for induction of cotton leaf curl disease. Virology (New York), 285(2), 234-243. doi: 10.1006/viro.2001.0949

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

Briddon, R. W., Stanley, J., 2006. Subviral agents associated with plant single-stranded DNA viruses. Virology , 344(1), 198-210. doi: 10.1016/j.virol.2005.09.042

Brown JK, 1992. Virus diseases. In: Cotton diseases. Hillocks RJ, ed. Wallingford, UK: CAB International, 275-329

Brown JK, 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 JK, 2010. Bemisia: Phylogenetic biology of the Bemisia tabaci sibling species group. In: Bemisia: Bionomics and Management of a Global Pest, [ed. by Stansly PA, Naranjo SE]. Netherlands: Springer. 31-67.

Brown JK, 2017. National Plant Disease Recovery System-Recovery Plan: Cotton leaf curl virus complex. USDA-ARS Office of Pest Management Policy, National Plant Disease Recovery System. http://www.ars.usda.gov/research/docs.htm?docid=14271

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 M.J, 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

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01/06/20  Updated by:

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

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