scholarly journals Interspecies recombination has driven the macroevolution of cassava mosaic begomoviruses

2021 ◽  
Author(s):  
Alvin Crespo-Bellido ◽  
J. Steen Hoyer ◽  
Divya Dubey ◽  
Ronica B. Jeannot ◽  
Siobain Duffy

Begomoviruses (family Geminiviridae , genus Begomovirus ) significantly hamper crop production and threaten food security around the world. The frequent emergence of new begomovirus genotypes is facilitated by high mutation frequencies and the propensity to recombine and reassort. Homologous recombination has been especially implicated in the emergence of novel cassava mosaic begomovirus (CMB) genotypes, which cause cassava mosaic disease (CMD). Cassava ( Manihot esculenta ) is a staple food crop throughout Africa, and an important industrial crop in Asia, two continents where production is severely constrained by CMD. The CMD species complex is comprised of 11 bipartite begomovirus species with ample distribution throughout Africa and the Indian subcontinent. While recombination is regarded as a frequent occurrence for CMBs, a revised, systematic assessment of recombination and its impact on CMB phylogeny is currently lacking. We assembled data sets of all publicly available, full-length DNA-A (n=880) and DNA-B (n=369) nucleotide sequences from the 11 recognized CMB species. Phylogenetic networks and complementary recombination detection methods revealed extensive recombination among the CMB sequences. Six out of the eleven species have descended from unique interspecies recombination events. Estimates of recombination and mutation rates revealed that all species experience mutation more frequently than recombination, but measures of population divergence indicate that recombination is largely responsible for the genetic differences between species. Our results support that recombination has significantly impacted the CMB phylogeny and has driven speciation in the CMD species complex. IMPORTANCE Cassava mosaic disease (CMD) is a significant threat to cassava production throughout Africa and Asia. CMD is caused by a complex comprised of 11 recognized virus species exhibiting accelerated rates of evolution, driven by high frequencies of mutation and genetic exchange. Here, we present a systematic analysis of the contribution of genetic exchange to cassava mosaic virus species-level diversity. Most of these species emerged as a result of genetic exchange. This is the first study to report the significant impact of genetic exchange on speciation in a group of viruses.

2021 ◽  
Author(s):  
Alvin Crespo-Bellido ◽  
John Steen Hoyer ◽  
Divya Dubey ◽  
Ronica B. Jeannot ◽  
Siobain Duffy

Begomoviruses (family Geminiviridae, genus Begomovirus) significantly hamper crop production and threaten food security around the world. The frequent emergence of new begomovirus genotypes is facilitated by high mutation frequencies and the propensity to recombine and reassort. Homologous recombination has been especially implicated in the emergence of novel cassava mosaic begomovirus (CMB) genotypes, which cause cassava mosaic disease (CMD). Cassava (Manihot esculenta) is a staple food crop throughout Africa, and an important industrial crop in Asia, two continents where production is severely constrained by CMD. The CMD species complex is comprised of 11 bipartite begomovirus species with ample distribution throughout Africa and the Indian subcontinent. While recombination is regarded as a frequent occurrence for CMBs, a revised, systematic assessment of recombination and its impact on CMB phylogeny is currently lacking. We assembled datasets of all publicly available, full-length DNA-A (n=880) and DNA-B (n=369) nucleotide sequences from the 11 recognized CMB species. Phylogenetic networks and complementary recombination detection methods revealed extensive recombination among the CMB sequences. Six out of the eleven species have descended from unique interspecies recombination events. Estimates of recombination and mutation rates revealed that all species experience mutation more frequently than recombination, but measures of population divergence indicate that recombination is largely responsible for the genetic differences between species. Our results support that recombination has significantly impacted the CMB phylogeny and is driving speciation in the CMD species complex.


Plant Disease ◽  
2021 ◽  
Author(s):  
Khonesavane Chittarath ◽  
Jenyfer Jimenez ◽  
Pinkham Vongphachanh ◽  
Ana Maria Leiva ◽  
Somkhit Sengsay ◽  
...  

Cassava (Manihot esculenta Crantz) has been traditionally grown as a subsistence crop in Laos, but in recent years cassava cultivation in this country has expanded and is becoming a ‘cash crop’ for farmers (Malik et al., 2020). This also means that cassava vegetative seed (stakes) is rapidly multiplied and distributed. One of the most important diseases affecting cassava in the world is the Cassava Mosaic Disease (CMD), caused by several species of begomoviruses and disseminated by infected stakes or vectored by the whitefly Bemisia tabaci (Legg et al., 2014). Sri Lankan cassava mosaic virus (SLCMV), a bipartite begomovirus, is the virus species causing CMD in Southeast Asia (SEA) and is widespread in Cambodia, Vietnam, Thailand and south China (Siriwan et al., 2020). During field surveys on July 12 to 14, 2020, the team in south Laos, surveyed 8 fields along the border with Cambodia, in the southern provinces of Attapeu and Champassack and identified CMD symptoms (Supplementary Figure 1A) in only one of the fields, located at Kong District of the Champassack province (GPS coordinates 13.94325, 105.99102). From these 8 fields, samples were collected from every third plant in an X pattern. Photographs from each sampled plant were taken and uploaded into CIAT’s PestDisPlace platform (https://pestdisplace.org), for CMD symptom confirmation (Supplementary Figure 1B). Leaf samples were sent to the laboratory for PCR using primers SLCMV-F 5’-ATGTCGAAGCGACCAGCAGATATAAT-3’ and SLCMV-R 5’-TTAATTGCTGACCGAATCGTAGAAG-3’ targeting the AV1 gene (Dutt et al., 2005), following the protocol described in Siriwan et al. (2020) and primers SLCMV-B-F1 5’-ACCGGATGGCCGCGCCCCCCTCT-3’ and SLCMV-B-606R 5’-CACCTACCCTGTTATCGCTAAG-3’ targeting part of the BV1 gene. Out of 60 samples collected for the field in Kong district, eleven (18.3%) resulted PCR positive to SLCMV (to DNA-A and DNA-B) but only four plants (6.7%) showed symptoms of CMD (see Supplementary Figure 1B and 1C). None of the samples in the other seven fields had CMD symptoms nor was SLCMV detected in any of these plants. Furthermore, the presence of CMD symptoms in the old leaves of the plants in the affected field suggests that the virus was introduced with contaminated stakes. The complete bipartite genome of one isolate (Champ1), was amplified by Rolling Circle Amplification and sequenced with the nanopore MinION technology as described by Leiva et al. (2020). The sequences were submitted to GenBank under accession nos MT946533 (DNA-A) and MT946534 (DNA-B). A phylogenetic tree for SLCMV and a link to the open SLCMV Nextstrain map (Hadfield et al., 2018) is included in Supplementary Figure 2. The sequences of the DNA-A and DNA-B components of the Champ1 isolate were nearly identical to those of anisolate of SLCMV from Ratanakiri, Cambodia (99.72% for DNA-A and 99.82 for DNA-B; Wang et al., 2016). Phylogenetic analysis (Supplementary Figure 2), grouped isolate Champ1 with those that form the cluster of SEA isolates that contain the shorter version of the rep gene (Siriwan et al., 2020). This short version of rep present a deletion of 7 amino acids at the C-terminus, which is involved in host responses to SLCMV (Wang et al., 2020). The confirmation of CMD and SLCMV in the border between Laos and Cambodia should be followed by disease containment and management strategies, particularly given that the majority cassava varieties grown in Laos are from neighbor countries, most of which have already reported the presence of CMD. Acknowledgements We thank all staff from the CIAT’s Cassava Program and the Plant Protection Center of Laos in Vientiane. We acknowledge financial support from the Australian Centre for International Agricultural Research (ACIAR) and the CGIAR Research Program on Roots, Tubers and Bananas (RTB) (https://www.cgiar.org/funders/).


2006 ◽  
Vol 87 (10) ◽  
pp. 3053-3065 ◽  
Author(s):  
Simon E. Bull ◽  
Rob W. Briddon ◽  
William S. Sserubombwe ◽  
Kahiu Ngugi ◽  
Peter G. Markham ◽  
...  

Cassava is a major factor in food security across sub-Saharan Africa. However, the crop is susceptible to losses due to biotic stresses, in particular to viruses of the genus Begomovirus (family Geminiviridae) that cause cassava mosaic disease (CMD). During the 1990s, an epidemic of CMD severely hindered cassava production across eastern and central Africa. A significant influence on the appearance of virus epidemics is virus diversity. Here, a survey of the genetic diversity of CMD-associated begomoviruses across the major cassava-growing areas of Kenya is described. Because an initial PCR-restriction fragment-length polymorphism analysis identified a much greater diversity of viruses than assumed previously, representative members of the population were characterized by sequence analysis. The full-length sequences of 109 components (68 DNA-A and 41 DNA-B) were determined, representing isolates of East African cassava mosaic virus and East African cassava mosaic Zanzibar virus, as well as a novel begomovirus species for which the name East African cassava mosaic Kenya virus is proposed. The DNA-B components were much less diverse than their corresponding DNA-A components, but nonetheless segregated into western and eastern (coastal) groups. All virus species and strains encountered showed distinct geographical distributions, highlighting the importance of preventing both the movement of viruses between these regions and the importation of the disease from adjacent countries and islands in the Indian Ocean that would undoubtedly encourage further diversification.


Plant Disease ◽  
1999 ◽  
Vol 83 (9) ◽  
pp. 877-877 ◽  
Author(s):  
S. K. Offei ◽  
M. Owuna-Kwakye ◽  
G. Thottappilly

Virus species causing cassava mosaic disease have been categorized into three classes based on their reaction with monoclonal antibodies (MAbs) and their distribution (2). These viruses have different, scarcely overlapping distribution: African cassava mosaic begomovirus (ACMV) occurs in Africa west of the Rift Valley and in South Africa; East African cassava mosaic (EACMV) occurs in Africa east of the Rift Valley and in Madagascar; and Indian cassava mosaic virus (ICMV) occurs in India and Sri Lanka (2). During 1998, surveys were conducted in farmers' fields in Ghana to assess the incidence and reaction of local cassava cultivars to cassava mosaic disease. Leaf samples from symptomatic plants were indexed by triple antibody sandwich-enzyme-linked immunosorbent assay with crude extracts and monoclonal antibodies obtained from the International Institute of Tropical Agriculture (IITA). Each sample was assayed with monoclonal antibody SCR 23, which detects ACMV and EACMV, SCR 33, which detects ACMV, and SCR 58, which detects ICMV. None of the samples reacted with SCR 58. Two of the samples collected from the western region of Ghana produced strong reactions with MAb SCR23 but did not react with ACMV-specific MAb SCR 33. This result was consistent in three separate experiments conducted on the samples, confirming that the virus was EACMV and not ACMV. The results extend the work by Ogbe et al. (1) and provide further evidence of the occurrence of EACMV in west Africa. References: (1) F. O. Ogbe et al. Plant Dis 83:398, 1999. (2) M. M. Swanson and B. D. Harrison. Trop. Sci. 34:15, 1994.


2007 ◽  
Vol 88 (12) ◽  
pp. 3458-3468 ◽  
Author(s):  
P. Lefeuvre ◽  
D. P. Martin ◽  
M. Hoareau ◽  
F. Naze ◽  
H. Delatte ◽  
...  

During the last few decades, many virus species have emerged, often forming dynamic complexes within which viruses share common hosts and rampantly exchange genetic material through recombination. Begomovirus species complexes are common and represent serious agricultural threats. Characterization of species complex diversity has substantially contributed to our understanding of both begomovirus evolution, and the ecological and epidemiological processes involved in the emergence of new viral pathogens. To date, the only extensively studied emergent African begomovirus species complex is that responsible for cassava mosaic disease. Here we present a study of another emerging begomovirus species complex which is associated with serious disease outbreaks in bean, tobacco and tomato on the south-west Indian Ocean (SWIO) islands off the coast of Africa. On the basis of 14 new complete DNA-A sequences, we describe seven new island monopartite begomovirus species, suggesting the presence of an extraordinary diversity of begomovirus in the SWIO islands. Phylogenetic analyses of these sequences reveal a close relationship between monopartite and bipartite African begomoviruses, supporting the hypothesis that either bipartite African begomoviruses have captured B components from other bipartite viruses, or there have been multiple B-component losses amongst SWIO virus progenitors. Moreover, we present evidence that detectable recombination events amongst African, Mediterranean and SWIO begomoviruses, while substantially contributing to their diversity, have not occurred randomly throughout their genomes. We provide the first statistical support for three recombination hot-spots (V1/C3 interface, C1 centre and the entire IR) and two recombination cold-spots (the V2 and the third quarter of V1) in the genomes of begomoviruses.


2021 ◽  
Vol 83 (8) ◽  
Author(s):  
F. Al Basir ◽  
Y. N. Kyrychko ◽  
K. B. Blyuss ◽  
S. Ray

AbstractMany plant diseases are caused by plant viruses that are often transmitted to plants by vectors. For instance, the cassava mosaic disease, which is spread by whiteflies, has a significant negative effect on plant growth and development. Since only mature whiteflies can contribute to the spread of the cassava mosaic virus, and the maturation time is non-negligible compared to whitefly lifetime, it is important to consider the effects this maturation time can have on the dynamics. In this paper, we propose a mathematical model for dynamics of cassava mosaic disease that includes immature and mature vectors and explicitly includes a time delay representing vector maturation time. A special feature of our plant epidemic model is that vector recruitment is negatively related to the delayed ratio between vector density and plant density. We identify conditions of biological feasibility and stability of different steady states in terms of system parameters and the time delay. Numerical stability analyses and simulations are performed to explore the role of various parameters, and to illustrate the behaviour of the model in different dynamical regimes. We show that the maturation delay may stabilise epidemiological dynamics that would otherwise be cyclic.


2021 ◽  
Vol 18 (1) ◽  
Author(s):  
Saengsoon Charoenvilaisiri ◽  
Channarong Seepiban ◽  
Mallika Kumpoosiri ◽  
Sombat Rukpratanporn ◽  
Nuchnard Warin ◽  
...  

Abstract Background Cassava mosaic disease (CMD) is one of the most devastating viral diseases for cassava production in Africa and Asia. Accurate yet affordable diagnostics are one of the fundamental tools supporting successful CMD management, especially in developing countries. This study aimed to develop an antibody-based immunoassay for the detection of Sri Lankan cassava mosaic virus (SLCMV), the only cassava mosaic begomovirus currently causing CMD outbreaks in Southeast Asia (SEA). Methods Monoclonal antibodies (MAbs) against the recombinant coat protein of SLCMV were generated using hybridoma technology. MAbs were characterized and used to develop a triple antibody sandwich enzyme-linked immunosorbent assay (TAS-ELISA) for SLCMV detection in cassava leaves and stems. Assay specificity, sensitivity and efficiency for SLCMV detection was investigated and compared to those of a commercial ELISA test kit and PCR, the gold standard. Results A TAS-ELISA for SLCMV detection was successfully developed using the newly established MAb 29B3 and an in-house polyclonal antibody (PAb) against begomoviruses, PAb PK. The assay was able to detect SLCMV in leaves, green bark from cassava stem tips, and young leaf sprouts from stem cuttings of SLCMV-infected cassava plants without cross-reactivity to those derived from healthy cassava controls. Sensitivity comparison using serial dilutions of SLCMV-infected cassava sap extracts revealed that the assay was 256-fold more sensitive than a commercial TAS-ELISA kit and 64-fold less sensitive than PCR using previously published SLCMV-specific primers. In terms of DNA content, our assay demonstrated a limit of detection of 2.21 to 4.08 × 106 virus copies as determined by quantitative real-time PCR (qPCR). When applied to field samples (n = 490), the TAS-ELISA showed high accuracy (99.6%), specificity (100%), and sensitivity (98.2%) relative to the results obtained by the reference PCR. SLCMV infecting chaya (Cnidoscolus aconitifolius) and coral plant (Jatropha multifida) was also reported for the first time in SEA. Conclusions Our findings suggest that the TAS-ELISA for SLCMV detection developed in this study can serve as an attractive tool for efficient, inexpensive and high-throughput detection of SLCMV and can be applied to CMD screening of cassava stem cuttings, large-scale surveillance, and screening for resistance.


2004 ◽  
Vol 53 (5) ◽  
pp. 577-584 ◽  
Author(s):  
J. Colvin ◽  
C. A. Omongo ◽  
M. N. Maruthi ◽  
G. W. Otim-Nape ◽  
J. M. Thresh

Viruses ◽  
2021 ◽  
Vol 13 (9) ◽  
pp. 1820
Author(s):  
Warren Freeborough ◽  
Nikki Gentle ◽  
Marie E. C. Rey

Among the numerous biological constraints that hinder cassava (Manihot esculenta Crantz) production, foremost is cassava mosaic disease (CMD) caused by virus members of the family Geminiviridae, genus Begomovirus. The mechanisms of CMD tolerance and susceptibility are not fully understood; however, CMD susceptible T200 and tolerant TME3 cassava landraces have been shown to exhibit different large-scale transcriptional reprogramming in response to South African cassava mosaic virus (SACMV). Recent identification of 85 MeWRKY transcription factors in cassava demonstrated high orthology with those in Arabidopsis, however, little is known about their roles in virus responses in this non-model crop. Significant differences in MeWRKY expression and regulatory networks between the T200 and TME3 landraces were demonstrated. Overall, WRKY expression and associated hormone and enriched biological processes in both landraces reflect oxidative and other biotic stress responses to SACMV. Notably, MeWRKY11 and MeWRKY81 were uniquely up and downregulated at 12 and 67 days post infection (dpi) respectively in TME3, implicating a role in tolerance and symptom recovery. AtWRKY28 and AtWRKY40 homologs of MeWRKY81 and MeWRKY11, respectively, have been shown to be involved in regulation of jasmonic and salicylic acid signaling in Arabidopsis. AtWRKY28 is an interactor in the RPW8-NBS resistance (R) protein network and downregulation of its homolog MeWRKY81 at 67 dpi in TME3 suggests a negative role for this WRKY in SACMV tolerance. In contrast, in T200, nine MeWRKYs were differentially expressed from early (12 dpi), middle (32 dpi) to late (67 dpi) infection. MeWRKY27 (homolog AtWRKY33) and MeWRKY55 (homolog AtWRKY53) were uniquely up-regulated at 12, 32 and 67 dpi in T200. AtWRKY33 and AtWRKY53 are positive regulators of leaf senescence and oxidative stress in Arabidopsis, suggesting MeWRKY55 and 27 contribute to susceptibility in T200.


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