Distinctive genetic structure and selection patterns in Plasmodium vivax from South Asia and East Africa

Ernest Diez Benavente; Emilia Manko; Jody Phelan; Monica Campos; Debbie Nolder; Diana Fernandez; Gabriel Velez-Tobon; Alberto Tobón Castaño; Jamille G Dombrowski; Claudio R F Marinho; Anna Caroline C Aguiar; Dhelio Batista Pereira; Kanlaya Sriprawat; Francois Nosten; Robert Moon; Colin J Sutherland; Susana Campino; Taane G Clark

doi:10.1038/s41467-021-23422-3

Distinctive genetic structure and selection patterns in Plasmodium vivax from South Asia and East Africa

Ernest Diez Benavente, Emilia Manko, Jody Phelan, Monica Campos, Debbie Nolder, Diana Fernandez, Gabriel Velez-Tobon, Alberto Tobón Castaño, Jamille G Dombrowski, Claudio R F Marinho, Anna Caroline C Aguiar, Dhelio Batista Pereira, Kanlaya Sriprawat, Francois Nosten, Robert Moon, Colin J Sutherland, Susana Campino, Taane G Clark

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Despite the high burden of Plasmodium vivax malaria in South Asian countries, the genetic diversity of circulating parasite populations is not well described. Determinants of antimalarial drug susceptibility for P. vivax in the region have not been characterised. Our genomic analysis of global P. vivax (n = 558) establishes South Asian isolates (n = 92) as a distinct subpopulation, which shares ancestry with some East African and South East Asian parasites. Signals of positive selection are linked to drug resistance-associated loci including pvkelch10, pvmrp1, pvdhfr and pvdhps, and two loci linked to P. vivax invasion of reticulocytes, pvrbp1a and pvrbp1b. Significant identity-by-descent was found in extended chromosome regions common to P. vivax from India and Ethiopia, including the pvdbp gene associated with Duffy blood group binding. Our investigation provides new understanding of global P. vivax population structure and genomic diversity, and genetic evidence of recent directional selection in this important human pathogen.

Original language	English
Article number	3160
Pages (from-to)	3160
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-23422-3
Publication status	Published - 26 May 2021
Externally published	Yes

Keywords

Africa, Eastern
Antimalarials/pharmacology
Asia
Drug Resistance/genetics
Duffy Blood-Group System
Genes, Protozoan
Genetic Loci
Humans
Malaria, Vivax/blood
Phylogeny
Phylogeography
Plasmodium vivax/drug effects
Polymorphism, Single Nucleotide
Protozoan Proteins/genetics
Reticulocytes/parasitology
Selection, Genetic

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10.1038/s41467-021-23422-3

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Benavente, E. D., Manko, E., Phelan, J., Campos, M., Nolder, D., Fernandez, D., Velez-Tobon, G., Castaño, A. T., Dombrowski, J. G., Marinho, C. R. F., Aguiar, A. C. C., Pereira, D. B., Sriprawat, K., Nosten, F., Moon, R., Sutherland, C. J., Campino, S., & Clark, T. G. (2021). Distinctive genetic structure and selection patterns in Plasmodium vivax from South Asia and East Africa. Nature Communications, 12(1), 3160. Article 3160. https://doi.org/10.1038/s41467-021-23422-3

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title = "Distinctive genetic structure and selection patterns in Plasmodium vivax from South Asia and East Africa",

abstract = "Despite the high burden of Plasmodium vivax malaria in South Asian countries, the genetic diversity of circulating parasite populations is not well described. Determinants of antimalarial drug susceptibility for P. vivax in the region have not been characterised. Our genomic analysis of global P. vivax (n = 558) establishes South Asian isolates (n = 92) as a distinct subpopulation, which shares ancestry with some East African and South East Asian parasites. Signals of positive selection are linked to drug resistance-associated loci including pvkelch10, pvmrp1, pvdhfr and pvdhps, and two loci linked to P. vivax invasion of reticulocytes, pvrbp1a and pvrbp1b. Significant identity-by-descent was found in extended chromosome regions common to P. vivax from India and Ethiopia, including the pvdbp gene associated with Duffy blood group binding. Our investigation provides new understanding of global P. vivax population structure and genomic diversity, and genetic evidence of recent directional selection in this important human pathogen.",

keywords = "Africa, Eastern, Antimalarials/pharmacology, Asia, Drug Resistance/genetics, Duffy Blood-Group System, Genes, Protozoan, Genetic Loci, Humans, Malaria, Vivax/blood, Phylogeny, Phylogeography, Plasmodium vivax/drug effects, Polymorphism, Single Nucleotide, Protozoan Proteins/genetics, Reticulocytes/parasitology, Selection, Genetic",

author = "Benavente, {Ernest Diez} and Emilia Manko and Jody Phelan and Monica Campos and Debbie Nolder and Diana Fernandez and Gabriel Velez-Tobon and Casta{\~n}o, {Alberto Tob{\'o}n} and Dombrowski, {Jamille G} and Marinho, {Claudio R F} and Aguiar, {Anna Caroline C} and Pereira, {Dhelio Batista} and Kanlaya Sriprawat and Francois Nosten and Robert Moon and Sutherland, {Colin J} and Susana Campino and Clark, {Taane G}",

note = "Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = may,

day = "26",

doi = "10.1038/s41467-021-23422-3",

language = "English",

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Benavente, ED, Manko, E, Phelan, J, Campos, M, Nolder, D, Fernandez, D, Velez-Tobon, G, Castaño, AT, Dombrowski, JG, Marinho, CRF, Aguiar, ACC, Pereira, DB, Sriprawat, K, Nosten, F, Moon, R, Sutherland, CJ, Campino, S & Clark, TG 2021, 'Distinctive genetic structure and selection patterns in Plasmodium vivax from South Asia and East Africa', Nature Communications, vol. 12, no. 1, 3160, pp. 3160. https://doi.org/10.1038/s41467-021-23422-3

TY - JOUR

T1 - Distinctive genetic structure and selection patterns in Plasmodium vivax from South Asia and East Africa

AU - Benavente, Ernest Diez

AU - Manko, Emilia

AU - Phelan, Jody

AU - Campos, Monica

AU - Nolder, Debbie

AU - Fernandez, Diana

AU - Velez-Tobon, Gabriel

AU - Castaño, Alberto Tobón

AU - Dombrowski, Jamille G

AU - Marinho, Claudio R F

AU - Aguiar, Anna Caroline C

AU - Pereira, Dhelio Batista

AU - Sriprawat, Kanlaya

AU - Nosten, Francois

AU - Moon, Robert

AU - Sutherland, Colin J

AU - Campino, Susana

AU - Clark, Taane G

PY - 2021/5/26

Y1 - 2021/5/26

N2 - Despite the high burden of Plasmodium vivax malaria in South Asian countries, the genetic diversity of circulating parasite populations is not well described. Determinants of antimalarial drug susceptibility for P. vivax in the region have not been characterised. Our genomic analysis of global P. vivax (n = 558) establishes South Asian isolates (n = 92) as a distinct subpopulation, which shares ancestry with some East African and South East Asian parasites. Signals of positive selection are linked to drug resistance-associated loci including pvkelch10, pvmrp1, pvdhfr and pvdhps, and two loci linked to P. vivax invasion of reticulocytes, pvrbp1a and pvrbp1b. Significant identity-by-descent was found in extended chromosome regions common to P. vivax from India and Ethiopia, including the pvdbp gene associated with Duffy blood group binding. Our investigation provides new understanding of global P. vivax population structure and genomic diversity, and genetic evidence of recent directional selection in this important human pathogen.

AB - Despite the high burden of Plasmodium vivax malaria in South Asian countries, the genetic diversity of circulating parasite populations is not well described. Determinants of antimalarial drug susceptibility for P. vivax in the region have not been characterised. Our genomic analysis of global P. vivax (n = 558) establishes South Asian isolates (n = 92) as a distinct subpopulation, which shares ancestry with some East African and South East Asian parasites. Signals of positive selection are linked to drug resistance-associated loci including pvkelch10, pvmrp1, pvdhfr and pvdhps, and two loci linked to P. vivax invasion of reticulocytes, pvrbp1a and pvrbp1b. Significant identity-by-descent was found in extended chromosome regions common to P. vivax from India and Ethiopia, including the pvdbp gene associated with Duffy blood group binding. Our investigation provides new understanding of global P. vivax population structure and genomic diversity, and genetic evidence of recent directional selection in this important human pathogen.

KW - Africa, Eastern

KW - Antimalarials/pharmacology

KW - Asia

KW - Drug Resistance/genetics

KW - Duffy Blood-Group System

KW - Genes, Protozoan

KW - Genetic Loci

KW - Humans

KW - Malaria, Vivax/blood

KW - Phylogeny

KW - Phylogeography

KW - Plasmodium vivax/drug effects

KW - Polymorphism, Single Nucleotide

KW - Protozoan Proteins/genetics

KW - Reticulocytes/parasitology

KW - Selection, Genetic

U2 - 10.1038/s41467-021-23422-3

DO - 10.1038/s41467-021-23422-3

M3 - Article

C2 - 34039976

SN - 2041-1723

VL - 12

SP - 3160

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 3160

ER -

Distinctive genetic structure and selection patterns in Plasmodium vivax from South Asia and East Africa

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Keywords

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