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Maintenance and expansion of genetic and trait variation following domestication in a clonal crop

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posted on 2024-05-02, 09:24 authored by Oliver W White, Manosh Kumar Biswas, Wendawek M Abebe, Yann Dussert, Firew Kebede, Richard A Nichols, Richard JA Buggs, Sebsebe Demissew, Feleke Woldeyes, Alexander ST Papadopulos, Trude Schwarzacher, Pat JS Heslop‐Harrison, Paul Wilkin, James S Borrell

Clonal propagation enables favourable crop genotypes to be rapidly selected and multiplied. However, the absence of sexual propagation can lead to low genetic diversity and accumulation of deleterious mutations, which may eventually render crops less resilient to pathogens or environmental change. To better understand this trade‐off, we characterize the domestication and contemporary genetic diversity of Enset (Ensete ventricosum), an indigenous African relative of bananas (Musa) and a principal starch staple for 20 million Ethiopians. Wild enset reproduction occurs strictly by sexual outcrossing, but for cultivation, it is propagated clonally and associated with diversification and specialization into hundreds of named landraces. We applied tGBS sequencing to generate genome‐wide genotypes for 192 accessions from across enset's cultivated distribution, and surveyed 1340 farmers on enset agronomic traits. Overall, reduced heterozygosity in the domesticated lineage was consistent with a domestication bottleneck that retained 37% of wild diversity. However, an excess of putatively deleterious missense mutations at low frequency present as heterozygotes suggested an accumulation of mutational load in clonal domesticated lineages. Our evidence indicates that the major domesticated lineages initially arose through historic sexual recombination associated with a domestication bottleneck, followed by the amplification of favourable genotypes through an extended period of clonal propagation. Among domesticated lineages, we found a significant phylogenetic signal for multiple farmer‐identified food, nutrition and disease resistance traits and little evidence of contemporary recombination. The development of future‐climate adapted genotypes may require crop breeding, but outcrossing risks exposing deleterious alleles as homozygotes. This trade‐off may partly explain the ubiquity and persistence of clonal propagation over recent centuries of comparative climate stability.

Funding

Landscape scale genomic-environment diversity data to model existing and novel agri-systems under climate change to enhance food security in Ethiopia

Biotechnology and Biological Sciences Research Council

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Modelling and genomics resources to enhance exploitation of the sustainable and diverse Ethiopian starch crop Enset and support livelihoods

Biotechnology and Biological Sciences Research Council

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Enhancing enset agriculture with mobile agri-data, knowledge interchange and climate adapted genotypes to support the Enset Center of Excellence

Biotechnology and Biological Sciences Research Council

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History

Author affiliation

College of Life Sciences/Genetics & Genome Biology

Version

  • VoR (Version of Record)

Published in

Molecular Ecology

Volume

32

Issue

15

Pagination

4165 - 4180

Publisher

Wiley

issn

0962-1083

eissn

1365-294X

Copyright date

2023

Available date

2024-05-02

Spatial coverage

England

Language

en

Deposited by

Professor Pat Heslop-Harrison

Deposit date

2024-04-27

Rights Retention Statement

  • No

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