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SNP-based genotyping and whole-genome sequencing reveal previously unknown genetic diversity in Xanthomonas vasicola pv. musacearum, causal agent of banana xanthomonas wilt, in its presumed Ethiopian origin.

ABSTRACT: For decades, Xanthomonas vasicola pv. musacearum (Xvm) has been an economically important bacterial pathogen on enset in Ethiopia. Since 2001, Xvm has also been responsible for significant losses to banana crops in several East and Central African countries, with devastating consequences for smallholder farmers. Understanding the genetic diversity within Xvm populations is essential for the smart design of transnationally reasoned, durable, and effective management practices. Previous studies have revealed limited genetic diversity in Xvm, with East African isolates from banana each falling into one of two closely related clades previously designated as sublineages SL 1 and SL 2, the former of which had also been detected on banana and enset in Ethiopia. Given the presumed origin of Xvm in Ethiopia, we hypothesized that both clades might be found in that country, along with additional genotypes not seen in Central and East African bananas. Genotyping of 97 isolates and whole-genome sequencing of 15 isolates revealed not only the presence of SL 2 in Ethiopia, but additional diversity beyond SL 1 and SL 2 in four new clades. Moreover, SL 2 was detected in the Democratic Republic of Congo, where previously SL 1 was the only clade reported. These results demonstrate a greater range of genetic diversity among Xvm isolates than previously reported, especially in Ethiopia, and further support the hypothesis that the East/Central Africa xanthomonas wilt epidemic has been caused by a restricted set of genotypes drawn from a highly diverse pathogen pool in Ethiopia.

SUBMITTER: Nakato GV

PROVIDER: S-EPMC7984043 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Xanthomonas vasicola pv. musacearum (Xvm) which causes Xanthomonas wilt (XW) on banana (Musa accuminata x balbisiana) and enset (Ensete ventricosum), is closely related to the species Xanthomonas vasicola that contains the pathovars vasculorum (Xvv) and holcicola (Xvh), respectively pathogenic to sugarcane and sorghum. Xvm is considered a monomorphic bacterium whose intra-pathovar diversity remains poorly understood. With the sudden emergence of Xvm within east and central Africa coupled with the unknown origin of one of the two sublineages suggested for Xvm, attention has shifted to adapting technologies that focus on identifying the origin and distribution of the genetic diversity within this pathogen. Although microbiological and conventional molecular diagnostics have been useful in pathogen identification. Recent advances have ushered in an era of genomic epidemiology that aids in characterizing monomorphic pathogens. To unravel the origin and pathways of the recent emergence of XW in Eastern and Central Africa, there was a need for a genotyping tool adapted for molecular epidemiology. Multi-Locus Variable Number of Tandem Repeat Analysis (MLVA) is able to resolve the evolutionary patterns and invasion routes of a pathogen. In this study, we identified microsatellite loci from nine published Xvm genome sequences. Of the 36 detected microsatellite loci, 21 were selected for primer design and 19 determined to be highly typeable, specific, reproducible and polymorphic with two- to four- alleles per locus on a sub-collection. The 19 markers were multiplexed and applied to genotype 335 Xvm strains isolated from seven countries over several years. The microsatellite markers grouped the Xvm collection into three clusters; with two similar to the SNP-based sublineages 1 and 2 and a new cluster 3, revealing an unknown diversity in Ethiopia. Five of the 19 markers had alleles present in both Xvm and Xanthomonas vasicola pathovars holcicola and vasculorum, supporting the phylogenetic closeliness of these three pathovars. Thank to the public availability of the haplotypes on the MLVABank database, this highly reliable and polymorphic genotyping tool can be further used in a transnational surveillance network to monitor the spread and evolution of XW throughout Africa.. It will inform and guide management of Xvm both in banana-based and enset-based cropping systems. Due to the suitability of MLVA-19 markers for population genetic analyses, this genotyping tool will also be used in future microevolution studies.

Project description:Banana production landscapes in the African Great Lakes Region (AGLR) have been under immense pressure from Xanthomonas wilt (XW) disease over the past two decades. XW, first reported on banana in central Uganda and eastern DR Congo in 2001, has since spread to the entire AGLR. XW is currently spreading westwards from hot spots in eastern DR Congo highlands, putting the plantain (Musa AAB genome) belt of central and west Africa at risk. In-depth understanding of the key variables responsible for disease spread, current hotspots, and vulnerable landscapes is crucial for disease early warning and management. We mapped aggregated disease distribution and hotspots in the AGLR and identified vulnerable landscapes across African banana production zones. Available data on disease prevalence collected over 11 years was regressed against environmental and expert developed covariates to develop the AGLR XW hotspots map. For the Africa-wide risk map, precipitation, distance to hotspots, degree of trade in fresh banana products, production zone interconnectedness and banana genotype composition were used as covariates. In the AGLR, XW was mainly correlated to precipitation and disease/banana management. Altitude and temperature had unexpectedly low effects, possibly due to an overriding impact of tool-mediated spread which is part of the management covariate. In the AGLR, the eastern part of DR Congo was a large hotspot with highest vulnerability. Apart from endemic zones in the AGLR and Ethiopia, northern Mozambique was perceived as a moderate risk zone mainly due to the predominance of 'Bluggoe' (Musa ABB type) which is highly susceptible to insect-vectored transmission. Presence of XW hotspots (e.g. eastern DR Congo) and vulnerable areas with low (e.g. north-western Tanzania) or no disease (e.g. Congo basin, western DR Congo and northern Mozambique) pressure suggest key areas where proactive measures e.g. quarantines and information sharing on XW diagnosis, epidemiology, and control could be beneficial.

Dataset Information

SNP-based genotyping and whole-genome sequencing reveal previously unknown genetic diversity in Xanthomonas vasicola pv. musacearum, causal agent of banana xanthomonas wilt, in its presumed Ethiopian origin.

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