Haplotype-based phylogenetic analysis and population genomics uncover the origin and domestication of sweetpotato

Mengxiao Yan; Ming Li; Yunze Wang; Xinyi Wang; M-Hossein Moeinzadeh; Dora G Quispe-Huamanquispe; Weijuan Fan; Yijie Fang; Yuqin Wang; Haozhen Nie; Zhangying Wang; Aiko Tanaka; Bettina Heider; Jan F Kreuze; Godelieve Gheysen; Hongxia Wang; Martin Vingron; Ralph Bock; Jun Yang

doi:10.1016/j.molp.2023.12.019

Haplotype-based phylogenetic analysis and population genomics uncover the origin and domestication of sweetpotato

Mol Plant. 2024 Feb 5;17(2):277-296. doi: 10.1016/j.molp.2023.12.019. Epub 2023 Dec 28.

Authors

Mengxiao Yan¹, Ming Li², Yunze Wang³, Xinyi Wang³, M-Hossein Moeinzadeh⁴, Dora G Quispe-Huamanquispe⁵, Weijuan Fan¹, Yijie Fang³, Yuqin Wang³, Haozhen Nie¹, Zhangying Wang⁶, Aiko Tanaka⁷, Bettina Heider⁸, Jan F Kreuze⁹, Godelieve Gheysen¹⁰, Hongxia Wang¹¹, Martin Vingron¹², Ralph Bock¹³, Jun Yang¹⁴

Affiliations

¹ Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai 201602, China.
² College of Life Sciences, Chongqing Normal University, Chongqing 401331, China; Biotechnology and Nuclear Technology Research Institute, Sichuan Academy of Agricultural Sciences, Chengdu 610061, China.
³ Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai 201602, China; College of Life Sciences, Shanghai Normal University, Shanghai 200234, China.
⁴ Department of Computational Molecular Biology, Max Planck Institute for Molecular Genetics, Ihnestraße 63-73, 14195 Berlin, Germany.
⁵ Department of Biotechnology, Ghent University, 9000 Ghent, Belgium.
⁶ Guangdong Provincial Key Laboratory of Crops Genetics and Improvement, Crop Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China.
⁷ Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan.
⁸ International Potato Center (CIP), Lima, Peru.
⁹ International Potato Center (CIP), Lima, Peru. Electronic address: j.kreuze@cgiar.org.
¹⁰ Department of Biotechnology, Ghent University, 9000 Ghent, Belgium. Electronic address: godelieve.gheysen@ugent.be.
¹¹ Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai 201602, China; CAS Center for Excellence of Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200233, China. Electronic address: hxwang@cemps.ac.cn.
¹² Department of Computational Molecular Biology, Max Planck Institute for Molecular Genetics, Ihnestraße 63-73, 14195 Berlin, Germany. Electronic address: vingron@molgen.mpg.de.
¹³ Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany. Electronic address: rbock@mpimp-golm.mpg.de.
¹⁴ Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai 201602, China; CAS Center for Excellence of Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200233, China. Electronic address: jyang03@cemps.ac.cn.

PMID: 38155570
DOI: 10.1016/j.molp.2023.12.019

Abstract

The hexaploid sweetpotato (Ipomoea batatas) is one of the most important root crops worldwide. However, its genetic origin remains controversial, and its domestication history remains unknown. In this study, we used a range of genetic evidence and a newly developed haplotype-based phylogenetic analysis to identify two probable progenitors of sweetpotato. The diploid progenitor was likely closely related to Ipomoea aequatoriensis and contributed the B₁ subgenome, IbT-DNA2, and the lineage 1 type of chloroplast genome to sweetpotato. The tetraploid progenitor of sweetpotato was most likely I. batatas 4x, which donated the B₂ subgenome, IbT-DNA1, and the lineage 2 type of chloroplast genome. Sweetpotato most likely originated from reciprocal crosses between the diploid and tetraploid progenitors, followed by a subsequent whole-genome duplication. In addition, we detected biased gene exchanges between the subgenomes; the rate of B₁ to B₂ subgenome conversions was nearly three times higher than that of B₂ to B₁ subgenome conversions. Our analyses revealed that genes involved in storage root formation, maintenance of genome stability, biotic resistance, sugar transport, and potassium uptake were selected during the speciation and domestication of sweetpotato. This study sheds light on the evolution of sweetpotato and paves the way for improvement of this crop.

Keywords: HPA; IbT-DNA; domestication; gene conversion; origin; sweetpotato.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Domestication
Genome, Plant*
Haplotypes
Metagenomics*
Phylogeny
Tetraploidy