Cassava whitefly species in eastern Nigeria and the threat of vector-borne pandemics from East and Central Africa

Bemisia tabaci (sensu latu) is a group of >40 highly cryptic whitefly species that are of global agricultural importance, both as crop pests and plant-virus vectors. Two devastating cassava diseases in East and Central Africa are spread by abundant populations of one of these species termed Sub-Saharan Africa 1 (SSA1). There is a substantive risk that these whitefly-borne pandemics will continue to spread westwards and disrupt cassava production for millions of smallholder farmers in West Africa. We report here, therefore, the first comprehensive survey of cassava B. tabaci in eastern Nigeria, a West African region likely to be the first affected by the arrival of these whitefly-borne pandemics. We found one haplotype comprising 32 individuals with 100% identical mtCO1 sequence to the East African SSA1 populations (previously termed SSA1-SG1) and 19 mtCO1 haplotypes of Sub-Saharan Africa 3 (SSA3), the latter being the most prevalent and widely distributed B. tabaci species in eastern Nigeria. A more divergent SSA1 mtCO1 sequence (previously termed SSA1-SG5) was also identified in the region, as were mtCO1 sequences identifying the presence of the MED ASL B. tabaci species and Bemisia afer. Although B. tabaci SSA1 was found in eastern Nigeria, they were not present in the high abundances associated with the cassava mosaic (CMD) and cassava brown streak disease (CBSD) pandemics of East and Central Africa. Also, no severe CMD or any CBSD symptoms were found in the region

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

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

Microbiome diversity and composition in Bemisia tabaci SSA1-SG1 whitefly are influenced by their host’s life stage

Within the Bemisia tabaci group of cryptic whitefly species, many are damaging agricultural pests and plant-virus vectors, conferring upon this group the status of one of the world’s top 100 most invasive and damaging ‘species’ that affect farmers’ income and livelihoods. Studies on the microbiome of whitefly life stages are scarce, although their composition and diversity greatly influence whitefly fitness and development. We used high-throughput sequencing to understand microbiome diversity in different developmental stages of the B. tabaci sub-Saharan Africa 1 (SSA1-SG1) species of the whitefly from Uganda. Endosymbionts (Portiera, Arsenophonus, Wolbachia and Hemipteriphilus were detected but excluded from the further statistical analysis as they were not influenced by life stage using( Permutational Multivariate Analysis of Variance Using Distance Matrices, (ADONIS, p= 0.925 and Bray, p = 0.903). Our results showed significant differences in the microbiome composition in different life stages of SSA1-SG1. The diversity was significantly higher in eggs (Shannon, p = 0.024; Simpson, p = 0.047) than that in nymphs and pupae, while the number of microbial species observed by the amplicon sequence variant (ASV) was not significant (n(ASV), p = 0.094). At the phylum and genus levels, the dominant constituents in the microbiome changed significantly at different developmental stages, with Halomonas being an egg-associated genus while Bacillus and Caldalkalibacillus were common in all life stages. These findings provide the first description of differing microbiome diversity in the life stage of whiteflies, suggesting their putative role in whitefly development

The molecular mechanisms that determine different degrees of polyphagy in the Bemisia tabaci species complex

The whitefly Bemisia tabaci is a closely related group of >35 cryptic species that feed on the phloem sap of a broad range of host plants. Species in the complex differ in their host‐range breadth, but the mechanisms involved remain poorly understood. We investigated, therefore, how six different B. tabaci species cope with the environmental unpredictability presented by a set of four common and novel host plants. Behavioral studies indicated large differences in performances on the four hosts and putative specialization of one of the species to cassava plants. Transcriptomic analyses revealed two main insights. First, a large set of genes involved in metabolism (>85%) showed differences in expression between the six species, and each species could be characterized by its own unique expression pattern of metabolic genes. However, within species, these genes were constitutively expressed, with a low level of environmental responsiveness (i.e., to host change). Second, within each species, sets of genes mainly associated with the super‐pathways “environmental information processing” and “organismal systems” responded to the host switching events. These included genes encoding for proteins involved in sugar homeostasis, signal transduction, membrane transport, and immune, endocrine, sensory and digestive responses. Our findings suggested that the six B. tabaci species can be divided into four performance/transcriptomic “Types” and that polyphagy can be achieved in multiple ways. However, polyphagy level is determined by the specific identity of the metabolic genes/pathways that are enriched and overexpressed in each species (the species' individual metabolic “tool kit”)

Ongoing geographical spread of Tomato yellow leaf curl virus

Tomato yellow leaf curl virus (TYLCV) seriously impacts tomato production throughout tropical and sub-tropical regions of the world. It has a broad geographical distribution and continues to spread to new regions in the Indian and Pacific Oceans including Australia, New Caledonia and Mauritius. We undertook a temporally-scaled, phylogeographic analysis of all publicly available, full genome sequences of TYLCV, together with 70 new genome sequences from Australia, Iran and Mauritius. This revealed that whereas epidemics in Australia and China likely originated through multiple independent viral introductions from the East-Asian region around Japan and Korea, the New Caledonian epidemic was seeded by a variant from the Western Mediterranean region and the Mauritian epidemic by a variant from the neighbouring island of Reunion. Finally, we show that inter-continental scale movements of TYLCV to East Asia have, at least temporarily, ceased, whereas long-distance movements to the Americas and Australia are probably still ongoing

A method for real-time classification of insect vectors of mosaic and brown streak disease in cassava plants for future implementation within a low-cost, handheld, in-field multispectral imaging sensor

Background The paper introduces a multispectral imaging system and data-processing approach for the identification and discrimination of morphologically indistinguishable cryptic species of the destructive crop pest, the whitefly Bemisia tabaci. This investigation and the corresponding system design, was undertaken in two phases under controlled laboratory conditions. The first exploited a prototype benchtop variant of the proposed sensor system to analyse four cryptic species of whitefly reared under similar conditions. The second phase, of the methodology development, employed a commercial high-precision laboratory hyperspectral imager to recover reference data from five cryptic species of whitefly, immobilized through flash freezing, and taken from across four feeding environments. Results The initial results, for the single feeding environment, showed that a correct species classification could be achieved in 85–95% of cases, utilising linear Partial Least Squares approaches. The robustness of the classification approach was then extended both in terms of the automated spatial extraction of the most pertinent insect body parts, to assist with the spectral classification model, as well as the incorporation of a non-linear Support Vector Classifier to maintain the overall classification accuracy at 88–98%, irrespective of the feeding and crop environment. Conclusion This study demonstrates that through an integration of both the spatial data, associated with the multispectral images being used to separate different regions of the insect, and subsequent spectral analysis of those sub-regions, that B. tabaci viral vectors can be differentiated from other cryptic species, that appear morphologically indistinguishable to a human observer, with an accuracy of up to 98%. The implications for the engineering design for an in-field, handheld, sensor system is discussed with respect to the learning gained from this initial stage of the methodology development

Additional File 6: Ensembl annotation of B. argentifolii and B. tabaci s.s genomes.

Genomic reannotation of the published B. argentifolii (doi.org/10.1186/s12915-016-0321-y) and B. tabaci s.s (doi.org/10.1093/gigascience/gix018) genomes using the Ensembl genebuild annotation pipeline; see here: https://www.ensembl.org/info/genome/genebuild/index.html  </p

Additional file 7: Endosymbiont assemblies and annotations

Candidatus Portiera aleyrodidarum (six populations of Bemisia tabaci s.l.), complete annotations and chromosome sequences.  Including custom script to help with Flye assembler output parsing. </p