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Mutations in DNA polymerase δ subunit 1 co-segregate with CMD2-type resistance to Cassava Mosaic Geminiviruses.

ABSTRACT: Cassava mosaic disease (CMD) suppresses cassava yields across the tropics. The dominant CMD2 locus confers resistance to cassava mosaic geminiviruses. It has been reported that CMD2-type landraces lose resistance after regeneration through de novo morphogenesis. As full genome bisulfite sequencing failed to uncover an epigenetic mechanism for this loss of resistance, whole genome sequencing and genetic variant analysis was performed and the CMD2 locus was fine-mapped to a 190 kilobase interval. Collectively, these data indicate that CMD2-type resistance is caused by a nonsynonymous, single nucleotide polymorphism in DNA polymerase δ subunit 1 (MePOLD1) located within this region. Virus-induced gene silencing of MePOLD1 in a CMD-susceptible cassava variety produced a recovery phenotype typical of CMD2-type resistance. Analysis of other CMD2-type cassava varieties identified additional candidate resistance alleles within MePOLD1. Genetic variation of MePOLD1, therefore, could represent an important genetic resource for resistance breeding and/or genome editing, and elucidating mechanisms of resistance to geminiviruses.

SUBMITTER: Lim YW

PROVIDER: S-EPMC9262879 | biostudies-literature | 2022 Jul

REPOSITORIES: biostudies-literature

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Mutations in DNA polymerase δ subunit 1 co-segregate with CMD2-type resistance to Cassava Mosaic Geminiviruses.

Lim Yi-Wen YW Mansfeld Ben N BN Schläpfer Pascal P Gilbert Kerrigan B KB Narayanan Narayanan N NN Qi Weihong W Wang Qi Q Zhong Zhenhui Z Boyher Adam A Gehan Jackson J Beyene Getu G Lin Zuh-Jyh Daniel ZD Esuma Williams W Feng Suhua S Chanez Christelle C Eggenberger Nadine N Adiga Gerald G Alicai Titus T Jacobsen Steven E SE Taylor Nigel J NJ Gruissem Wilhelm W Bart Rebecca S RS

Nature communications 20220707 1

Cassava mosaic disease (CMD) suppresses cassava yields across the tropics. The dominant CMD2 locus confers resistance to cassava mosaic geminiviruses. It has been reported that CMD2-type landraces lose resistance after regeneration through de novo morphogenesis. As full genome bisulfite sequencing failed to uncover an epigenetic mechanism for this loss of resistance, whole genome sequencing and genetic variant analysis was performed and the CMD2 locus was fine-mapped to a 190 kilobase interval. ...[more]

PMID: 35798722

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Project description:BackgroundCassava mosaic disease (CMD) in Madagascar is caused by a complex of at least six African cassava mosaic geminivirus (CMG) species. This provides a rare opportunity for a comparative study of the evolutionary and epidemiological dynamics of distinct pathogenic crop-infecting viral species that coexist within the same environment. The genetic and spatial structure of CMG populations in Madagascar was studied and Bayesian phylogeographic modelling was applied to infer the origins of Madagascan CMG populations within the epidemiological context of related populations situated on mainland Africa and other south western Indian Ocean (SWIO) islands.ResultsThe isolation and analysis of 279 DNA-A and 117 DNA-B sequences revealed the presence in Madagascar of four prevalent CMG species (South African cassava mosaic virus, SACMV; African cassava mosaic virus, ACMV; East African cassava mosaic Kenya virus, EACMKV; and East African cassava mosaic Cameroon virus, EACMCV), and of numerous CMG recombinants that have, to date, only ever been detected on this island. SACMV and ACMV, the two most prevalent viruses, displayed low degrees of genetic diversity and have most likely been introduced to the island only once. By contrast, EACMV-like CMG populations (consisting of East African cassava mosaic virus, EAMCKV, EACMCV and complex recombinants of these) were more diverse, more spatially structured, and displayed evidence of at least three independent introductions from mainland Africa. Although there were no statistically supported virus movement events between Madagascar and the other SWIO islands, at least one mainland African ACMV variant likely originated in Madagascar.ConclusionsOur study highlights both the complexity of CMD in Madagascar, and the distinct evolutionary and spatial dynamics of the different viral species that collectively are associated with this disease. Given that more distinct CMG species and recombinants have been found in Madagascar than any other similarly sized region of the world, the risks of recombinant CMG variants emerging on this island are likely to be higher than elsewhere. Evidence of an epidemiological link between Madagascan and mainland African CMGs suggests that the consequences of such emergence events could reach far beyond the shores of this island.

Project description:Cassava is infected by numerous geminiviruses in Africa and India that cause devastating losses to poor farmers. We here describe the molecular diversity of seven representative cassava mosaic geminiviruses (CMGs) infecting cassava from multiple locations in Tanzania. We report for the first time the presence of two isolates in East Africa: (EACMCV-[TZ1] and EACMCV-[TZ7]) of the species East African cassava mosaic Cameroon virus, originally described in West Africa. The complete nucleotide sequence of EACMCV-[TZ1] DNA-A and DNA-B components shared a high overall sequence identity to EACMCV-[CM] components (92% and 84%). The EACMCV-[TZ1] and -[TZ7] genomic components have recombinations in the same genome regions reported in EACMCV-[CM], but they also have additional recombinations in both components. Evidence from sequence analysis suggests that the two strains have the same ancient origin and are not recent introductions. EACMCV-[TZ1] occurred widely in the southern part of the country. Four other CMG isolates were identified: two were close to the EACMV-Kenya strain (named EACMV-[KE/TZT] and EACMV-[KE/TZM] with 96% sequence identity); one isolate, TZ10, had 98% homology to EACMV-UG2Svr and was named EACMV-UG2 [TZ10]; and finally one isolate was 95% identical to EACMV-[TZ] and named EACMV-[TZ/YV]. One isolate of African cassava mosaic virus with 97% sequence identity with other isolates of ACMV was named ACMV-[TZ]. It represents the first ACMV isolate from Tanzania to be sequenced. The molecular variability of CMGs was also evaluated using partial B component nucleotide sequences of 13 EACMV isolates from Tanzania. Using the sequences of all CMGs currently available, we have shown the presence of a number of putative recombination fragments that are more prominent in all components of EACMV than in ACMV. This new knowledge about the molecular CMG diversity in East Africa, and in Tanzania in particular, has led us to hypothesize about the probable importance of this part of Africa as a source of diversity and evolutionary change both during the early stages of the relationship between CMGs and cassava and in more recent times. The existence of multiple CMG isolates with high DNA genome diversity in Tanzania and the molecular forces behind this diversity pose a threat to cassava production throughout the African continent.

Project description:Growing cassava in Africa requires resistance against the viruses causing cassava mosaic disease (CMD) and the viruses causing cassava brown streak disease (CBSD). A dominant CMD2 resistance gene from a West African cassava landrace provides strong resistance against the cassava mosaic viruses. However, resistance against cassava brown streak viruses is limited to cassava varieties that show tolerance to the disease. A recently identified cassava germplasm that cannot be infected with cassava brown streak viruses provides a new source of the resistance required to protect cassava from CBSD. We present a synopsis of the status of virus resistance in cassava and report on the research to combine resistance against CBSD and CMD. We improve the lengthy and erratic screening for CBSD resistance by proposing a virus infection and screening protocol for the viruses causing CBSD and CMD, which allows a rapid and precise assessment of cassava resistance under controlled conditions. Using this approach, we classified the virus responses of cassava lines from Africa and South America and identified truly virus-resistant clones that cannot be infected with any of the known viruses causing CBSD even under the most stringent virus infections. A modification of this protocol was used to test seedlings from cassava crosses for resistance against both diseases. A broad-spectrum resistance was identified in a workflow that lasted 9 months from seed germination to the identification of virus resistance. The workflow we propose dramatically reduces the evaluation and selection time required in a classical breeding workflow to reach the advanced field trial stage in only 9 months by conducting selections for virus resistance and plant multiplication in parallel. However, it does not bypass field evaluations; cassava resistance assessment prior to the field limits the evaluation to candidates with virus resistance defined as the absence of symptoms and the absence of the virus. The transfer of our virus screening workflow to cassava breeding programs enhances the efficiency by which resistance against viruses can be selected. It provides a precise definition of the plant's resistance response and can be used as a model system to tackle resistance in cassava against other diseases.

Dataset Information

Mutations in DNA polymerase δ subunit 1 co-segregate with CMD2-type resistance to Cassava Mosaic Geminiviruses.

Publications

Mutations in DNA polymerase δ subunit 1 co-segregate with CMD2-type resistance to Cassava Mosaic Geminiviruses.

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