African cassava mosaic virus
(African cassava mosaic)

Pictures

Picture	Title	Caption	Copyright
Title Symptoms Caption Cassava mosaic disease (African cassava mosaic); whole plant, showing Cassava mosaic symptoms. Copyright ©CABI/Phil Taylor	Symptoms	Cassava mosaic disease (African cassava mosaic); whole plant, showing Cassava mosaic symptoms.	©CABI/Phil Taylor
Title Symptoms Caption Cassava mosaic disease (African cassava mosaic); symptoms on cassava leaf. Copyright ©CABI/Phil Taylor	Symptoms	Cassava mosaic disease (African cassava mosaic); symptoms on cassava leaf.	©CABI/Phil Taylor
Title Symptoms Caption Cassava mosaic disease (African cassava mosaic); symptoms on cassava. Copyright ©Pasquale Piccirillo	Symptoms	Cassava mosaic disease (African cassava mosaic); symptoms on cassava.	©Pasquale Piccirillo

Identity

Preferred Scientific Name

• African cassava mosaic virus

Preferred Common Name

• African cassava mosaic

Other Scientific Names

• Cassava African mosaic bigeminivirus

International Common Names

• English: cassava latent virus; cassava mosaic
• Spanish: mosaico africano de la yuca
• French: mosaïque africaine du manioc

Local Common Names

• Germany: Cassava Mosaikvirus

English acronym

• ACMV

EPPO code

• ACMV00 (African cassava mosaic begomovirus)

Summary of Invasiveness

Cassava is vegetatively propagated therefore ACMV and other CMGs are primarily transmitted via movement of contaminated cuttings. Consequently, introductions of specific CMGs into new localities mirror patterns of cassava cuttings exchange among farmers. Once infected cuttings are planted, the virus establishes easily and can be transmitted within and between fields through the feeding behaviour of the whitefly vector, Bemisia tabaci. ACMV is particularly invasive in that it is the most widespread of all known CMGs, occurring across all cassava-producing countries of Africa in cassava and several alternative host plants (Thottappilly et al., 2003; Alabi et al. 2015). ACMV has also been reported infecting non-cultivated exotic cotton species in Pakistan (Nawaz-Ul-Rehman et al., 2012) further underscoring its invasive nature. Yield loss due to CMD can range from 12 to 82%, depending on the cassava variety and infection type (Owor et al., 2004). ACMV is not on the IUCN or ISSG alert list.

Taxonomic Tree

• Domain: Virus
•     Unknown: "ssDNA viruses"
•         Unknown: "DNA viruses"
•             Family: Geminiviridae
•                 Genus: Begomovirus
•                     Species: African cassava mosaic virus

Notes on Taxonomy and Nomenclature

African cassava mosaic virus (ACMV) is a member of the genus Begomovirus in the family Geminiviridae. ACMV was the first of 10 recognized and one tentative begomovirus species characterized from cassava plants affected by cassava mosaic disease (CMD). Historically, the first report of CMD came from the Usambaras Mountains range in northeast Tanzania in 1894. The disease was named as ‘Kräuselkrankheit’, a German word that translates to ‘rippling/crinkling illness’ (Warbug, 1894) which describes symptoms observed on affected plants. Although a virus was originally suggested to be the causal agent of CMD (Zimmermann, 1906) and its transmission by Bemisia spp. whiteflies demonstrated (Chant, 1958), it was not until the 1970s when small, quasi-isometric, geminate particles were found in leaf tissue samples from symptomatic CMD-affected cassava (Harrison et al., 1977). The virus was momentarily named as cassava latent virus (CLV) because its sap inoculation into Nicotiana clevelandii did not produce symptoms in this herbaceous host (Bock et al., 1978). Following the molecular characterization of CLV (Stanley and Gay, 1983), the virus was successful sap-inoculated onto N. benthamiana and cassava and typical CMD symptoms produced (Bock and Woods, 1983) thus fulfilling Koch’s postulates and prompting a name change from CLV to ACMV. Fifteen years later, an infectious clone of ACMV was developed and its infectivity onto cassava via biolistic inoculation achieved (Briddon et al., 1998). Over the course of several decades, nine additional viruses and one tentative species have been characterized from CMD-affected cassava worldwide. They are: East African cassava mosaic virus (EACMV; Hong et al., 1993), East African cassava mosaic Malawi virus (EACMMV; Zhou et al., 1998), South African cassava mosaic virus (SACMV; Berrie et al., 1998), East African cassava mosaic Cameroon virus (EACMCV; Fondong et al., 2000), Indian cassava mosaic virus (ICMV; Mathew and Muniyappa, 1992; Saunders et al., 2002), Sri Lankan cassava mosaic virus (SLCMV; Saunders et al., 2002), East African cassava mosaic Zanzibar virus (EACMZV; Maruthi et al., 2004), East African cassava mosaic Kenya virus (EACMKV; Bull et al., 2006) and Cassava mosaic Madagascar virus (CMMGV; Harimalala et al., 2012). A recombinant virus, African cassava mosaic Burkina Faso virus (ACMBFV; Tiendrébéogo et al., 2012) was also characterized from disease-affected cassava but is yet to be recognized as a bona fide species by the International Committee on Taxonomy of Viruses (ICTV). Besides ICMV and SLCMV, all other CMD-associated viruses are of African origin. All CMD-associated viruses are collectively called cassava mosaic geminiviruses (CMGs) or cassava mosaic begomoviruses (CMBs).

Description

The first elucidation of ACMV was achieved when electron micrographs obtained from sap extracts from symptomatic cassava leaves revealed twinned (geminate), small, quasi-isometric particles measuring 15-20 nm in diameter (Harrison et al., 1977; Böttcher et al., 2004). The particle size measures 20 x 30 nm and comprises a 30 kDa coat protein (Stanley et al., 2005). The coat protein encapsidates the bipartite, circular ssDNA DNA A and DNA B genome components of ACMV that are each ~2.7 Kb.

Both genome components are needed for efficient transmission of ACMV and its establishment in otherwise healthy cassava plants (Liu et al., 1997). Once the vector has acquired the virus, a 6-8 hour latent period must elapse before the vector can transmit the virus over an inoculation access period of 20-30 minutes (Dubern, 1994). After acquiring the virus, viruliferous whiteflies remain infective for 9 days but progenies of infective whiteflies do not retain the virus (Dubern, 1994). Thus ACMV is transstadially, but not transovarially, transmitted (Dubern, 1994). Compared with the Asian Bemisia tabaci, the African B. tabaci is more efficient in transmitting CMGs from Africa than those from Asia suggesting a phenomenon of virus-vector-co-adaptation within the cassava pathosystem (Maruthi et al., 2002). Apart from B. tabaci, other whitefly species such as Bemisia afer are known to transmit ACMV (Palaniswami et al., 1996) albeit at a lower efficiency.

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.

History of Introduction and Spread

ACMV is thought to be native to the African continent and its islands. Although the primary host, cassava, was introduced to Africa from South America in the sixteenth and eighteenth centuries, ACMV has not been reported in the Americas but its disease symptoms were first reported in Tanzania in the nineteenth century (Warbug, 1894) and the causal pathogen studied (Storey, 1936; Storey and Nichols, 1938; Bock and Woods, 1983). In mainland Africa, ACMV occurs in virtually all cassava-growing regions spanning East Africa (Legg, 1999; Ndunguru et al., 2005, 2016; Bull et al., 2006), West and Central Africa (Fauquet and Fargette, 1990; Fondong et al. 2000; Ogbe et al., 2003, 2006; Alabi, 2009) and Southern Africa (Mabasa, 2007; Cossa, 2011; Chikoti et al., 2013; Mulenga et al., 2016). In the 1930s, ACMV symptoms on cassava plants were noticed in Madagascar (Cours et al., 1997) and its distribution alongside other CMGs mapped (Harimalala et al., 2015). Several reports of ACMV in Seychelles, Zanzibar and other islands exist (Fauquet and Fargette, 1990; Thresh and Cooter, 2005). ACMV has a relatively stable genome with fewer species than EACMV-type CMGs but recently a tentative ACMV-like recombinant begomovirus, African cassava mosaic Burkina Faso virus (ACMBFV) was characterized in Burkina Faso (Tiendrébéogo et al., 2012) indicating plasticity of the ACMV genome.

Risk of Introduction

Cassava is a vegetatively propagated crop and this mode of propagation is exploited by CMGs, their genetic variants and sequences enhancing geminivirus symptoms (SEGS) for their spread distal to the infection loci. As most farmers have little or no knowledge of the viral aetiology of symptomatic plants, there is a high frequency of farmer-to-farmer exchange of virus-infected planting material and CMGs take advantage of this to launch into CMD-free areas (Alabi et al., 2015). This is arguably the primary route for spread of ACMV across most cassava-growing regions.  

Secondarily, CMGs are also acquired and transmitted from virus-infected plants to healthy plants through the feeding behaviour of the whitefly vector, Bemisia tabaci. However, this occurs over short distances (within field) because B. tabaci is a ‘weak’ flier (Chant, 1958; Dubern, 1994). However, aided by the direction of the prevailing wind, whiteflies can spread CMGs over long distances within and between fields (Fargette et al., 1990). Studies have shown that B.tabaci populations from specific geographical regions exhibit lower virus transmission efficiency (Maruthi et al., 2002) with the consequence that huge whitefly populations are more important in the spread of ACMV than the transmission efficiency of individual insects (Legg, 2010). But the population dynamics of B. tabaci is influenced by many factors including environmental and biological factors as well as abundance of susceptible cassava varieties. High whitefly populations are therefore highly likely in countries with a biannual rainfall pattern that fosters continuous ‘green bridges’ for perpetuation of the whitefly’s preferred cassava foliar stages for feeding and reproduction. This is probably the more likely reason for the pandemic spread of the more severe form of CMD in East Africa. Once introduced into a new area, CMD eradication is difficult because besides cassava, there are known wild hosts of ACMV and the other CMGs that also support substantial whitefly pest densities (Alabi et al., 2015).

Hosts/Species Affected

ACMV, like the other CMGs, are primarily borne in cassava vegetative cuttings. Emerging leaves from such cuttings may manifest CMD symptoms and serve as sources of virus inoculum for secondary spread within and across fields by the whitefly vector. True cassava seeds are not known to carry the virus (Dubern, 1994). Depending on the mode of infection, symptoms appear in the first emerging leaves for cutting infection and 12-20 days after inoculation by viruliferous whiteflies (Storey and Nichols, 1938) usually determined by varietal characteristics.

Host Plants and Other Plants Affected

Growth Stages

Symptoms

CMGs cause a variety of foliar symptoms on cassava but no pattern is ascribed to any one single virus. Generally, symptoms include yellow or green mosaic, mottling, and misshapen and twisted leaflets (Thottappilly et al., 2003; Alabi et al., 2011). The display of the symptoms may vary in distribution in the fields, from plant to plant and even on the same plant. The pattern of foliar symptoms is influenced by the associated virus species, the presence of sequences enhancing geminivirus symptoms (SEGS) (Ndunguru et al., 2016) and the presence of single or mixed infections, age of the plant, variety responses to infection and environmental factors (Legg and Thresh, 2000; Maruthi et al., 2002; Ogbe et al., 2003). Studies have shown that severe symptoms are usually characteristic of plants infected by mixtures of CMGs, their recombinant variants and/or SEGS. This was evident in plants infected by ACMV/ East African cassava mosaic Uganda variant (EACMV-UG) first recorded in Uganda in the 1990s (Zhou et al., 1998). EACMV-UG is a recombinant virus that arose from recombination of portions of the genomes of ACMV and EACMV (Zhou et al., 1997). The time to symptom expression in an infected plant depend on the mode of infection. Planting material sourced from infected stock display ACMV symptoms in the first few emerging leaves (cutting-borne infection) whereas ACMV infections facilitated by whiteflies (vector-borne infection) require a lag period before the virus titre can build up to levels capable of eliciting symptoms.

Field diagnosis of CMD symptoms may be confusing especially if the fields are also infested with cassava green mites (CGMs); with symptoms looking more severe than normal. Although CMGs affect cassava plants to varying levels of severity, the symptoms produced cannot easily be ascribed to any one virus species by visual inspection of diseased leaves. This is because the mosaic symptoms do not form characteristic patterns associated with specific viruses. In infection complexes, therefore, it is important to confirm the causal species through PCR and ELISA methods.

List of Symptoms/Signs

Means of Movement and Dispersal

Vector transmission (biotic)

Vector transmission is the most important and efficient means of within field transmission of ACMV from infected plants to healthy ones. The virus is transmitted in a non-persistent manner and transmission can be optimal with as few as 10 viruliferous whiteflies (Dubern, 1994). Vector mobility is key in ACMV transmission over short (within field) and long (between fields) distances and is aided by wind direction (Fargette et al., 1990).

Accidental introduction

This is not known to be a factor in introduction of ACMV to virus-free areas.

Intentional introduction

There is no information on the intentional introduction of ACMV to new areas, but the literature indicates that most farmers are unfamiliar with the viral aetiology of symptomatic plants, with the consequence that they are oblivious to the presence of the disease in the selection of commonly shared or traded planting materials (Alabi et al., 2015). This is arguably the most important route of movement of ACMV and other CMGs across regions.

Pathway Causes

Pathway Vectors

Plant Trade

Vectors and Intermediate Hosts

Impact Summary

Economic Impact

The economic impact of ACMV as a single virus is not clearly stated in the literature. However, collectively CMGs have been shown to cause varying levels of yield loss depending on whether they occur as single or mixed infections and the susceptibility of varieties infected (Owor et al., 2004). Because of the difficulty of measuring yield loss attributed only to ACMV or to CMGs, the majority of yield loss estimates were conducted in the twentieth century (Thresh et al., 1994; Thottappilly et al., 2003; Legg et al., 2004). At the time, annual yield loss estimates were approximated at 15% and 24% translating to 12-23 million tonnes or US$ 1.2-2.3 billion (Thresh et al., 1997). In other studies, yield loss estimates were revised upwards to 30% in a region-wide assessment of sub-Saharan Africa (Legg and Thresh, 2000; Legg et al., 2006).

Social Impact

CMD-related yield loss not only impacts crop performance but disrupts the livelihoods of people that depend on cassava as a staple. This was evident in East Africa when a regional pandemic of an unusually severe form of CMD began in Uganda in the early to mid-1990s (Gibson et al., 1996; Otim-Nape et al., 1997) and spread across the East African region causing severe crop loss. The East African CMD pandemic resulted in famine-related deaths (Otim-Nape et al., 1998) reminiscent of the infamous potato late blight disease outbreak in Ireland in the nineteenth century (Alabi et al., 2015).

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
• Highly adaptable to different environments
• Is a habitat generalist
• Tolerant of shade
• Has high genetic variability

• Altered trophic level
• Host damage
• Increases vulnerability to invasions
• Negatively impacts agriculture
• Negatively impacts livelihoods
• Negatively impacts trade/international relations

• Rooting

• Highly likely to be transported internationally accidentally
• Highly likely to be transported internationally illegally
• Difficult/costly to control

Diagnosis

Distinct foliar mosaic symptoms induced by virus infection of cassava plants can be used for visual diagnosis of CMD but identification of the CMGs involved in the disease requires serological and/or molecular assays.

For purposes of detection, ACMV can be detected using polyclonal antibodies applied in Enzyme-linked immunosorbent assay (ELISA) in Double antibody sandwich (DAS) ELISA formats capable of detecting the virus in leaf extracts (Sequeira and Harrison, 1982). Monoclonal antibodies capable of discriminating CMGs can be used for rapid detection of CMGs using Triple- antibody sandwich-ELISA (Thomas et al., 1986). The different forms of ELISA are versatile and can be used to screen large field samples but they are of limited use for the discrimination of mixed virus infections due to similarities in coat protein epitopes of CMGs (Thottapilly et al., 2003). Mixed virus infections can be detected and diagnosed using polymerase chain reaction (PCR) methods in singleplex (Fondong et al., 2000; Berry and Rey, 2001; Pita et al., 2001; Ndunguru et al., 2005; Ogbe et al., 2006; Alabi et al., 2008; Sserubombwe et al., 2008; Monde et al., 2010) and multiplex (Ndunguru et al., 2005; Ogbe et al., 2006; Alabi et al., 2008; Abarshi et al., 2012; Aloyce et al., 2013) formats. 

Detection and Inspection

Symptoms caused by ACMV are not distinguishable from those caused by other CMGs by visual inspection. However, mosaic patterns on cassava leaves indicate the presence of one or more of the CMD causal viruses, which can be discriminated using various diagnostic tools described under Diagnosis.

Similarities to Other Species/Conditions

ACMV and other CMGs are indistinguishable from each other on the basis of foliar symptoms. Serological assays also have limitations for distinguishing CMGs. ACMV and other CMGs can best be distinguished using molecular approaches with virus-specific oligonucleotides.

Prevention and Control

Approaches to CMD management have been discussed in several review articles (Atiri et al., 2004; Thresh and Cooter et al., 2005; Vanderschuren et al., 2007). They include crop resistance, CMD avoidance and cultural control, vector management, monitoring and survey.

Crop Resistance

Over the years, conventional breeding for resistance to ACMV and other CMGs has been the main thrust for prevention and control of cassava mosaic disease (Thresh and Cooter, 2005; Dixon et al., 2001, 2010). In the initial stages of breeding efforts, various sources of resistance were identified but Manihoti glaziovii was initially the sole candidate resistance gene source (Jennings, 1994). Later efforts included cassava landraces in the resistance gene pool (Fregene et al., 2001). Crosses between different cassava varieties mainly from West Africa resulted in the generation of tropical Manihot species (TMS) and tropical Manihot esculenta (TME) that were considerably resistant to CMGs and were pivotal in the control of the severe form of CMD in East Africa (Legg et al., 2006). These materials were shared with many national breeding programmes in Africa for inclusion in local breeding programmes. Recently, to complement conventional breeding, efforts have been made in the development of transgenic resistance to CMD (Vanderschuren et al., 2007; 2009; Sayre et al., 2011)

Avoidance and Cultural Control

This is probably the cheapest way of managing ACMV and CMD in resource poor farmers’ fields. It involves planting of virus-free cassava cuttings obtained from a careful selection of plant materials from older crops observed to be disease-free in the previous season. Other approaches include roguing of diseased plants in the early stages of crop growth, disease avoidance by adjusting dates of planting, intercropping and varietal mixture. Results obtained from applying these management strategies have been viewed differently. Some have deemed the strategies effective (Sserubombwe et al., 2001; Fondong et al., 2002; Thresh and Otim-Nape, 1994), whereas others have disputed their effectiveness (Fargette and Fauquet, 1988; Otim-Nape et al., 1997). Despite disagreements, such methods have found application with varying levels of success.

Vector Management

Chemical control of whiteflies to limit the spread of ACMV has not been widely adopted by farmers in Africa mainly due to the cost of chemicals. Biological control using parasitoids has remained at an experimental level with little to show for effective delivery of whitefly control to minimize the spread of CMGs (Legg et al., 2014, and references therein).  

Monitoring and Survey

In order to monitor changes in the CMD dynamics across sub-Saharan Africa, several surveillances have been and continue to be conducted (Ndunguru et al., 2005; Bull et al., 2006; Ogbe et al., 2006; Sserubombwe et al., 2008; De Bruyn et al., 2012; Harimalala et al., 2012; Muengula-Manyi et al., 2012; Zinga et al., 2012; Chikoti et al., 2013; Mulenga et al., 2016). Results from these efforts have informed decisions made by government authorities in addressing the CMD disease burden in farmers’ fields via deployment of disease-resistant cultivars.

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Organizations

Nigeria: International Institute of Tropical Agriculture (IITA), PMB 5320, Ibadan, Oyo State, www.iita.org

Nigeria: National Root Crops Research Institute (NRCRI), Umudike Rd, Umudike, http://www.nrcri.gov.ng

Uganda: National Agricultural Research Organisation (NARO), P.O. Box 295 Entebbe Berkeley Rd, Entebbe , https://www.naro.go.ug/

USA: Donald Danforth Plant Science Center, 975 North Warson Road, St. Louis, Missouri, https://www.danforthcenter.org/

Colombia: International Center for Tropical Agriculture (CIAT), Km 17, Recta Cali-Palmira, Valle del Cauca, http://ciat.cgiar.org/

Contributors

09/10/17 Original text by:

Olufemi Joseph Alabi, Department of Plant Pathology & Microbiology, Texas A&M AgriLife Research & Extension Center, Weslaco, Texas, USA

Rabson M. Mulenga, Zambia Agriculture Research Institute, Mount Makulu Central Research Station, Chilanga, Lusaka, Zambia

Distribution Maps