Origin of domesticated water chestnuts (Trapa bispinosa Roxb.) and genetic variation in wild water chestnuts

Abstract The water chestnut Trapa bispinosa Roxb. has been domesticated in China and has been reported as the only domesticated species of this genus. To understand the origin of T. bispinosa and its evolution pathway, we compared the genetic similarity and seed morphology of domesticated water ches...

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Main Authors: Dinh Thi Lam, Taro Kataoka, Hiroki Yamagishi, Guoping Sun, Tetsuro Udatsu, Katsunori Tanaka, Ryuji Ishikawa
Format: Article
Language:English
Published: Wiley 2024-02-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.10925
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author Dinh Thi Lam
Taro Kataoka
Hiroki Yamagishi
Guoping Sun
Tetsuro Udatsu
Katsunori Tanaka
Ryuji Ishikawa
author_facet Dinh Thi Lam
Taro Kataoka
Hiroki Yamagishi
Guoping Sun
Tetsuro Udatsu
Katsunori Tanaka
Ryuji Ishikawa
author_sort Dinh Thi Lam
collection DOAJ
description Abstract The water chestnut Trapa bispinosa Roxb. has been domesticated in China and has been reported as the only domesticated species of this genus. To understand the origin of T. bispinosa and its evolution pathway, we compared the genetic similarity and seed morphology of domesticated water chestnut T. bispinosa with three wild species T. natans, T. incisa, and T. japonica along with archeological seed samples from the Tianluoshan site (approximately 7000–6300 cal BP) in China. The largest seed size was observed only in the domesticated species, whereas other wild species showed smaller size including T. natans L. genetically close to the domesticated type, and T. incisa was the smallest in size. The volumes of the seed capsule and endosperm were measured using X ray CT scans, showing the ratios of total volumes between T. bispinosa and wild species ranged from 4.2 to 4.5. The ratios of endosperm volume ranged from 3.3 to 3.7. Both measurements showed domesticated species have larger seed volume. Genome size was indirectly estimated by flow cytometry. Domesticated species with larger seed size was estimated as diploid, as were the wild species except for tetraploid species T. japonica. Domesticated species clearly showed the largest edible organs, but it was not a result of ploidy level changes. Maternal lineages traced using complete whole chloroplast sequences, suggested that T. natans is the closest to T. bispinosa, both of which are close to T. japonica. The result was confirmed by PCR genotyping with chloroplast insertion/deletion (cpINDEL) markers developed in the study. T. incisa showed distinct plastid types within the species, and T. japonica showed a unique plastid genotype. Our study concludes the largest volumes for the edible endosperm have been accomplished through nearly 6000 years of artificial selection, but the domestication did not involve ploidy level changes.
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spelling doaj.art-34d06d23ca294c3c9d1c01baabceb5262024-02-29T08:56:40ZengWileyEcology and Evolution2045-77582024-02-01142n/an/a10.1002/ece3.10925Origin of domesticated water chestnuts (Trapa bispinosa Roxb.) and genetic variation in wild water chestnutsDinh Thi Lam0Taro Kataoka1Hiroki Yamagishi2Guoping Sun3Tetsuro Udatsu4Katsunori Tanaka5Ryuji Ishikawa6Faculty of Agriculture and Life Science Hirosaki University Hirosaki Aomori JapanFaculty of Humanity and Social Science Hirosaki University Hirosaki Aomori JapanFaculty of Agriculture and Life Science Hirosaki University Hirosaki Aomori JapanZhejiang Provincial Research Institute of Cultural Relics and Archaeology Hangzhou ChinaFaculty of Agriculture Miyazaki University Miyazaki JapanFaculty of Agriculture and Life Science Hirosaki University Hirosaki Aomori JapanFaculty of Agriculture and Life Science Hirosaki University Hirosaki Aomori JapanAbstract The water chestnut Trapa bispinosa Roxb. has been domesticated in China and has been reported as the only domesticated species of this genus. To understand the origin of T. bispinosa and its evolution pathway, we compared the genetic similarity and seed morphology of domesticated water chestnut T. bispinosa with three wild species T. natans, T. incisa, and T. japonica along with archeological seed samples from the Tianluoshan site (approximately 7000–6300 cal BP) in China. The largest seed size was observed only in the domesticated species, whereas other wild species showed smaller size including T. natans L. genetically close to the domesticated type, and T. incisa was the smallest in size. The volumes of the seed capsule and endosperm were measured using X ray CT scans, showing the ratios of total volumes between T. bispinosa and wild species ranged from 4.2 to 4.5. The ratios of endosperm volume ranged from 3.3 to 3.7. Both measurements showed domesticated species have larger seed volume. Genome size was indirectly estimated by flow cytometry. Domesticated species with larger seed size was estimated as diploid, as were the wild species except for tetraploid species T. japonica. Domesticated species clearly showed the largest edible organs, but it was not a result of ploidy level changes. Maternal lineages traced using complete whole chloroplast sequences, suggested that T. natans is the closest to T. bispinosa, both of which are close to T. japonica. The result was confirmed by PCR genotyping with chloroplast insertion/deletion (cpINDEL) markers developed in the study. T. incisa showed distinct plastid types within the species, and T. japonica showed a unique plastid genotype. Our study concludes the largest volumes for the edible endosperm have been accomplished through nearly 6000 years of artificial selection, but the domestication did not involve ploidy level changes.https://doi.org/10.1002/ece3.10925chloroplast genomeflow cytometrygenome contentmaternal lineagewater chestnuts
spellingShingle Dinh Thi Lam
Taro Kataoka
Hiroki Yamagishi
Guoping Sun
Tetsuro Udatsu
Katsunori Tanaka
Ryuji Ishikawa
Origin of domesticated water chestnuts (Trapa bispinosa Roxb.) and genetic variation in wild water chestnuts
Ecology and Evolution
chloroplast genome
flow cytometry
genome content
maternal lineage
water chestnuts
title Origin of domesticated water chestnuts (Trapa bispinosa Roxb.) and genetic variation in wild water chestnuts
title_full Origin of domesticated water chestnuts (Trapa bispinosa Roxb.) and genetic variation in wild water chestnuts
title_fullStr Origin of domesticated water chestnuts (Trapa bispinosa Roxb.) and genetic variation in wild water chestnuts
title_full_unstemmed Origin of domesticated water chestnuts (Trapa bispinosa Roxb.) and genetic variation in wild water chestnuts
title_short Origin of domesticated water chestnuts (Trapa bispinosa Roxb.) and genetic variation in wild water chestnuts
title_sort origin of domesticated water chestnuts trapa bispinosa roxb and genetic variation in wild water chestnuts
topic chloroplast genome
flow cytometry
genome content
maternal lineage
water chestnuts
url https://doi.org/10.1002/ece3.10925
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