Endemism and reemergence potential of the ipomovirus Sweet potato mild mottle virus (family Potyviridae) in Eastern Africa: half a century of mystery

Viruses have the ability to frequently colonize new hosts and ecological niches because of their inherently high genetic and evolutionary plasticity. However, a virus may emerge and remain of no or less economic importance until changes in viral and/or environmental factors dictate its epidemiological status. An example is sweet potato mild mottle virus (SPMMV), which was first reported in the 1970s on sweetpotatoes in eastern Africa, has remained endemic in the region and poorly understood, yet accounting for 60-95% losses especially in mixed infections. Unlike other sweetpotato viruses which have a global incidence, SPMMV has never been confirmed outside eastern Africa. This implicates the region as its center of origin, but does not fully account for SPMMV’s exclusive geographic delimitation to eastern Africa. Despite its importance, several mysteries and research gaps surround SPMMV, which decelerate efforts for effective virus disease management in sweetpotato. The aim of this review is to articulate research gaps, propose pivotal scientific directions and stimulate knowledge generation for better management of virus diseases in sweetpotato. Vector-mediated transmission of SPMMV remains enigmatic. Here we postulate testable hypotheses to explain SPMMV transmission. Comparisons between SPMMV and cassava brown streak ipomoviruses demonstrate epidemiological “hallmarks” for monitoring SPMMV. Evolutionary forces on SPMMV coupled with the virus’ broad host range imply a ‘silent build up’ of better fit variants in a changing climate, and this could explode into a worse disease conundrum. These information gaps need urgent filling to ease future management of virus disease emergences in sweetpotato

Distribution of Bemisia tabaci in different agro-ecological regions in Uganda and the threat of vector-borne pandemics into new cassava growing areas

Previous studies in sub-Saharan Africa have showed the spread of cassava mosaic disease (CMD) and cassava brown streak disease (CBSD) pandemics into different cassava growing regions by high Bemisia tabaci populations. Studies did indicate that there were stark differences in some whitefly species, yet they have not looked extensively across agroecologies. Members of B. tabaci species complex termed sub-Saharan Africa 1 (SSA1) and SSA2 have been linked to the spread of CMD and CBSD viruses. During the period of a severe CMD pandemic in the 1990s, SSA2 was the most predominant until the resurgence of SSA1, particularly SSA1-subgroup1 (SSA1-SG1) from the early 2000s to date. Cassava being a drought resilient crop has become an important food security crop and has been introduced into new areas and regions. Considering the role B. tabaci in the spread of cassava virus pandemics into neighboring regions, we investigated the genetic diversity and distribution of B. tabaci in nine different agro-ecological regions of Uganda in 2017. Adult whiteflies were collected from cassava and 33 other host plants from cassava-growing areas, those with limited cassava and areas with no cassava, where it is being introduced as a food security crop. The partial sequences of the mitochondrial cytochrome oxidase 1 (mtCO1) gene (657 bp) were used to determine the phylogenetic relationships between the sampled B. tabaci. Cassava B. tabaci SSA1 (-SG1, -SG2, -Hoslundia (previously called SSA1-SG1/2), -SG3), SSA2 and SSA3; non-cassava B. tabaci SSA6, SSA10, SSA11, SSA12, SSA13, MED-ASL, MED-Q1, MEAM1, Indian Ocean; and other Bemisia species, Bemisia afer and Bemisia Uganda1 were identified in the study. SSA3, one of the key B. tabaci species that occurs on cassava in West Africa, was identified for the first time in Uganda. The SSA1-SG1 was widely distributed, predominated on cassava and was found on 17 other host-plants. The ability of SSA1-SG1 to exist in environments with limited or no cassava growing poses the risk of continued spread of virus pandemics. Therefore, measures must be put in place to prevent the introduction of diseased materials into new areas, since the vectors exist

What has changed in the outbreaking populations of the severe crop pest whitefly species in cassava in two decades?

High populations of African cassava whitefly (Bemisia tabaci) have been associated with epidemics of two viral diseases in Eastern Africa. We investigated population dynamics and genetic patterns by comparing whiteflies collected on cassava in 1997, during the first whitefly upsurges in Uganda, with collections made in 2017 from the same locations. Nuclear markers and mtCOI barcoding sequences were used on 662 samples. The composition of the SSA1 population changed significantly over the 20-year period with the SSA1-SG2 percentage increasing from 0.9 to 48.6%. SSA1-SG1 and SSA1-SG2 clearly interbreed, confirming that they are a single biological species called SSA1. The whitefly species composition changed: in 1997, SSA1, SSA2 and B. afer were present; in 2017, no SSA2 was found. These data and those of other publications do not support the ‘invader’ hypothesis. Our evidence shows that no new species or new population were found in 20 years, instead, the distribution of already present genetic clusters composing SSA1 species have changed over time and that this may be in response to several factors including the introduction of new cassava varieties or climate changes. The practical implications are that cassava genotypes possessing both whitefly and disease resistances are needed urgently

Occurrence of Bondar's Nesting Whitefly, Paraleyrodes bondari (Hemiptera: Aleyrodidae), on cassava in Uganda

Cassava is a valued calorific source to millions of Africans who eat it daily and a vital staple for their foodsecurity. One of the key constraints to this crop is whiteflies which are both a vector of viral diseasesand a direct pest. Although the African cassava whitefly is known to cause physical damage on cassavawith considerable tuberous yield loss, a recent whitefly outbreak caused unusually severe damage, whichprompted the current reported investigation. Molecular identification of whitefly adults sampled fromthe affected cassava field revealed the presence of a new whitefly species, Paraleyrodes bondari. Thiscommunication is the first report of the occurrence of P. bondari on cassava in Uganda

Genetic diversity of whitefly (Bemisia spp.) on crop and uncultivated plants in Uganda: implications for the control of this devastating pest species complex in Africa

Over the past three decades, highly increased whitefly (Bemisia tabaci) populations have been observed on the staple food crop cassava in eastern Africa and associated with ensuing viral disease pandemics and food insecurity. Increased whitefly numbers have also been observed in other key agricultural crops and weeds. Factors behind the population surges on different crops and their interrelationships are unclear, although in cassava they have been associated with specific populations within the Bemisia tabaci species complex known to infest cassava crops in Africa. This study carried out an in-depth survey to understand the distribution of B. tabaci populations infesting crops and uncultivated plant hosts in Uganda, a centre of origin for this pest complex. Whitefly samples were collected from 59 identified plant species and 25 unidentified weeds in a countrywide survey. Identities of 870 individual adult whiteflies were determined through mitochondrial cytochrome oxidase 1 sequences (651 bp) in the 3′ barcode region used for B. tabaci systematics. Sixteen B. tabaci and five related whitefly putative species were identified based on > 4.0% nucleotide divergence, of which three are proposed as novel B. tabaci putative species and four as novel closely related whitefly species. The most prevalent whiteflies were classified as B. tabaci MED-ASL (30.5% of samples), sub-Saharan Africa 1 (SSA1, 22.7%) and Bemisia Uganda1 (12.1%). These species were also indicated to be the most polyphagous occurring on 33, 40 and 25 identified plant species, respectively. Multiple (≥ 3) whitefly species occurred on specific crops (bean, eggplant, pumpkin and tomato) and weeds (Sida acuta and Ocimum gratissimum). These plants may have increased potential to act as reservoirs for mixed infections of whitefly-vectored viruses. Management of whitefly pest populations in eastern Africa will require an integration of approaches that consider their degree of polyphagy and a climate that enables the continuous presence of crop and uncultivated plant hosts

Review and guide to a future naming system of African Bemisia tabaci species

Once a pest has been correctly identified, its genus and species name can provide a link to valuable indications of its ecology, biology and life history that are critical for developing control strategies. Importantly, this link should exist even when the pest was known under other names (synonyms), or was not considered a pest at all (National Research Council, 1968). Many examples have shown that incorrect identification or classification of a pest has led to fruitless searches for biocontrol agents in the native range, incorrect assignments as disease vectors, and costly, yet misdirected, suppression measures. As new approaches for delimiting species based on molecular information become more widely used, the process of correctly identifying a species has become even more complex. Fortunately, we have good systematic frameworks and nomenclatural systems that are able to cope with these challenges. Here we review challenges associated with classification and identification within the Bemisia tabaci (Gennadius) species complex. These pests and the viruses they transmit have emerged in the past few decades as among the most damaging to food and fibre crops globally (Varma & Malathi, 2003; Pimental et al., 2005; Seal et al., 2006), especially in sub‐Saharan Africa (SSA). The systematics of the B. tabaci species group has been a highly debated topic for years (Boykin, 2014). Putative species are indistinguishable morphologically, so other biological data have been collected to investigate the species in the complex. Based on genetic differences (Colvin et al., 2004; Sseruwagi et al., 2005; Boykin et al., 2007; Boykin et al., 2013; Hsieh et al., 2014) and mating incompatibility (Colvin et al., 2004; Liu et al., 2007; Xu et al., 2010), B. tabaci is now recognized as a species complex that consists of at least 34 putative species (Boykin et al., 2012). The rapid discovery of significant species diversity has led to many changes in the informal names used over the last 10 years (Boykin, 2014), creating confusion in the literature

Expansion of the cassava brown streak pandemic in Uganda revealed by annual field survey data for 2004 to 2017

Funder: Uganda Government Association for Strengthening Agricultural Research in Eastern and Central AfricaFunder: Bill and Melinda Gates Foundation (Bill & Melinda Gates Foundation)Abstract: Cassava brown streak disease (CBSD) is currently the most devastating cassava disease in eastern, central and southern Africa affecting a staple crop for over 700 million people on the continent. A major outbreak of CBSD in 2004 near Kampala rapidly spread across Uganda. In the following years, similar CBSD outbreaks were noted in countries across eastern and central Africa, and now the disease poses a threat to West Africa including Nigeria - the biggest cassava producer in the world. A comprehensive dataset with 7,627 locations, annually and consistently sampled between 2004 and 2017 was collated from historic paper and electronic records stored in Uganda. The survey comprises multiple variables including data for incidence and symptom severity of CBSD and abundance of the whitefly vector (Bemisia tabaci). This dataset provides a unique basis to characterize the epidemiology and dynamics of CBSD spread in order to inform disease surveillance and management. We also describe methods used to integrate and verify extensive field records for surveys typical of emerging epidemics in subsistence crops

Crowdsourcing Real-Time Viral Disease and Pest Information: A Case of Nation-Wide Cassava Disease Surveillance in a Developing Country

In most developing countries, a huge proportion of the national food basket is supported by small subsistence agricultural systems. A major challenge to these systems is disease and pest attacks which have a devastating effect on the small-holder farmers that depend on these systems for their livelihoods. A key component of any proposed solution is a good disease surveillance network. However, current surveillance efforts are unable to provide sufficient data for monitoring such phenomena over a vast geographic area efficiently and effectively due to limited resources, both human and financial. Crowdsourcing with farmer crowds that have access to mobile phones offers a viable option to provide all year round real-time surveillance data on viral disease and pest incidence and severity. This work presents a mobile ad hoc surveillance system for monitoring viral diseases and pests in cassava. We present results from a pilot in Uganda where this system was deployed for 76 weeks. We discuss the participation behaviours of the crowds with mobile smartphones as well as the effects of several incentives applied

Endemism and Reemergence Potential of the Ipomovirus Sweet Potato Mild Mottle Virus (Family Potyviridae) in Eastern Africa: Half a Century of Mystery

Viruses have the ability to frequently colonize new hosts and ecological niches because of their inherently high genetic and evolutionary plasticity. However, a virus may emerge and remain of no or less economic importance until changes in viral or environmental factors dictate its epidemiological status. An example is sweet potato mild mottle virus (SPMMV), which was first reported in the 1970s on sweetpotato in eastern Africa. SPMMV has remained endemic in the region and poorly understood, yet accounting for 60 to 95% of losses, especially in mixed infections. Unlike other sweetpotato viruses which have global incidences, SPMMV has never been confirmed outside eastern Africa. This implicates the region as its center of origin but does not fully account for SPMMV's exclusive geographic delimitation to eastern Africa. Despite its importance, several mysteries and research gaps surround SPMMV, which decelerate efforts for effective virus disease management in sweetpotato. The aim of this review is to articulate research gaps, propose pivotal scientific directions, and stimulate knowledge generation for better management of virus diseases in sweetpotato. Vector-mediated transmission of SPMMV remains enigmatic. Here, we postulate testable hypotheses to explain SPMMV transmission. Comparisons between SPMMV and cassava brown streak ipomoviruses demonstrate epidemiological “hallmarks” for monitoring SPMMV. Evolutionary forces on SPMMV coupled with the virus' broad host range imply a “silent build up” of more fit variants in a changing climate, and this could explode into a worse disease conundrum. These information gaps need urgent filling to ease future management of virus disease emergences in sweetpotato. [Graphic: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license