The Jujube Genome Provides Insights into Genome Evolution and the Domestication of Sweetness/Acidity Taste in Fruit Trees

Jujube (Ziziphus jujuba Mill.) belongs to the Rhamnaceae family and is a popular fruit tree species with immense economic and nutritional value. Here, we report a draft genome of the dry jujube cultivar 'Junzao' and the genome resequencing of 31 geographically diverse accessions of cultiva...

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Published inPLoS genetics Vol. 12; no. 12; p. e1006433
Main Authors Huang, Jian, Zhang, Chunmei, Zhao, Xing, Fei, Zhangjun, Wan, KangKang, Zhang, Zhong, Pang, Xiaoming, Yin, Xiao, Bai, Yang, Sun, Xiaoqing, Gao, Lizhi, Li, Ruiqiang, Zhang, Jinbo, Li, Xingang
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.12.2016
Public Library of Science (PLoS)
Subjects
Acids
Bioinformatics
Biology and Life Sciences
Chromosome Mapping
Colleges & universities
Domestication
Engineering
Evolution
Evolution, Molecular
Fruit - genetics
Fruits
Genome, Plant
Genomes
Genomics
Germplasm
Metabolism
Microsatellite Repeats - genetics
Molecular Sequence Annotation
Phylogeny
Research and Analysis Methods
Rhamnaceae
Rosaceae
Rosales
Sequence Alignment
Taste - genetics
Trees
Ziziphus
Ziziphus - genetics
Beijing China
New York
China
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Abstract Jujube (Ziziphus jujuba Mill.) belongs to the Rhamnaceae family and is a popular fruit tree species with immense economic and nutritional value. Here, we report a draft genome of the dry jujube cultivar 'Junzao' and the genome resequencing of 31 geographically diverse accessions of cultivated and wild jujubes (Ziziphus jujuba var. spinosa). Comparative analysis revealed that the genome of 'Dongzao', a fresh jujube, was ~86.5 Mb larger than that of the 'Junzao', partially due to the recent insertions of transposable elements in the 'Dongzao' genome. We constructed eight proto-chromosomes of the common ancestor of Rhamnaceae and Rosaceae, two sister families in the order Rosales, and elucidated the evolutionary processes that have shaped the genome structures of modern jujubes. Population structure analysis revealed the complex genetic background of jujubes resulting from extensive hybridizations between jujube and its wild relatives. Notably, several key genes that control fruit organic acid metabolism and sugar content were identified in the selective sweep regions. We also identified S-locus genes controlling gametophytic self-incompatibility and investigated haplotype patterns of the S locus in the jujube genomes, which would provide a guideline for parent selection for jujube crossbreeding. This study provides valuable genomic resources for jujube improvement, and offers insights into jujube genome evolution and its population structure and domestication.
AbstractList Jujube (Ziziphus jujuba Mill.) belongs to the Rhamnaceae family and is a popular fruit tree species with immense economic and nutritional value. Here, we report a draft genome of the dry jujube cultivar 'Junzao' and the genome resequencing of 31 geographically diverse accessions of cultivated and wild jujubes (Ziziphus jujuba var. spinosa). Comparative analysis revealed that the genome of 'Dongzao', a fresh jujube, was ~86.5 Mb larger than that of the 'Junzao', partially due to the recent insertions of transposable elements in the 'Dongzao' genome. We constructed eight proto-chromosomes of the common ancestor of Rhamnaceae and Rosaceae, two sister families in the order Rosales, and elucidated the evolutionary processes that have shaped the genome structures of modern jujubes. Population structure analysis revealed the complex genetic background of jujubes resulting from extensive hybridizations between jujube and its wild relatives. Notably, several key genes that control fruit organic acid metabolism and sugar content were identified in the selective sweep regions. We also identified S-locus genes controlling gametophytic self-incompatibility and investigated haplotype patterns of the S locus in the jujube genomes, which would provide a guideline for parent selection for jujube crossbreeding. This study provides valuable genomic resources for jujube improvement, and offers insights into jujube genome evolution and its population structure and domestication.
Jujube (Ziziphus jujuba Mill.) belongs to the Rhamnaceae family and is a popular fruit tree species with immense economic and nutritional value. Here, we report a draft genome of the dry jujube cultivar 'Junzao' and the genome resequencing of 31 geographically diverse accessions of cultivated and wild jujubes (Ziziphus jujuba var. spinosa). Comparative analysis revealed that the genome of 'Dongzao', a fresh jujube, was ~86.5 Mb larger than that of the 'Junzao', partially due to the recent insertions of transposable elements in the 'Dongzao' genome. We constructed eight proto-chromosomes of the common ancestor of Rhamnaceae and Rosaceae, two sister families in the order Rosales, and elucidated the evolutionary processes that have shaped the genome structures of modern jujubes. Population structure analysis revealed the complex genetic background of jujubes resulting from extensive hybridizations between jujube and its wild relatives. Notably, several key genes that control fruit organic acid metabolism and sugar content were identified in the selective sweep regions. We also identified S-locus genes controlling gametophytic self-incompatibility and investigated haplotype patterns of the S locus in the jujube genomes, which would provide a guideline for parent selection for jujube crossbreeding. This study provides valuable genomic resources for jujube improvement, and offers insights into jujube genome evolution and its population structure and domestication.Jujube (Ziziphus jujuba Mill.) belongs to the Rhamnaceae family and is a popular fruit tree species with immense economic and nutritional value. Here, we report a draft genome of the dry jujube cultivar 'Junzao' and the genome resequencing of 31 geographically diverse accessions of cultivated and wild jujubes (Ziziphus jujuba var. spinosa). Comparative analysis revealed that the genome of 'Dongzao', a fresh jujube, was ~86.5 Mb larger than that of the 'Junzao', partially due to the recent insertions of transposable elements in the 'Dongzao' genome. We constructed eight proto-chromosomes of the common ancestor of Rhamnaceae and Rosaceae, two sister families in the order Rosales, and elucidated the evolutionary processes that have shaped the genome structures of modern jujubes. Population structure analysis revealed the complex genetic background of jujubes resulting from extensive hybridizations between jujube and its wild relatives. Notably, several key genes that control fruit organic acid metabolism and sugar content were identified in the selective sweep regions. We also identified S-locus genes controlling gametophytic self-incompatibility and investigated haplotype patterns of the S locus in the jujube genomes, which would provide a guideline for parent selection for jujube crossbreeding. This study provides valuable genomic resources for jujube improvement, and offers insights into jujube genome evolution and its population structure and domestication.
Jujube ( Ziziphus jujuba Mill.) belongs to the Rhamnaceae family and is a popular fruit tree species with immense economic and nutritional value. Here, we report a draft genome of the dry jujube cultivar ‘Junzao’ and the genome resequencing of 31 geographically diverse accessions of cultivated and wild jujubes ( Ziziphus jujuba var. spinosa ). Comparative analysis revealed that the genome of ‘Dongzao’, a fresh jujube, was ~86.5 Mb larger than that of the ‘Junzao’, partially due to the recent insertions of transposable elements in the ‘Dongzao’ genome. We constructed eight proto-chromosomes of the common ancestor of Rhamnaceae and Rosaceae, two sister families in the order Rosales, and elucidated the evolutionary processes that have shaped the genome structures of modern jujubes. Population structure analysis revealed the complex genetic background of jujubes resulting from extensive hybridizations between jujube and its wild relatives. Notably, several key genes that control fruit organic acid metabolism and sugar content were identified in the selective sweep regions. We also identified S-locus genes controlling gametophytic self-incompatibility and investigated haplotype patterns of the S locus in the jujube genomes, which would provide a guideline for parent selection for jujube crossbreeding. This study provides valuable genomic resources for jujube improvement, and offers insights into jujube genome evolution and its population structure and domestication. A balanced sweetness and acidity taste is among the most important characteristics of fruits. It is generally believed that human selection of sweetness plays a crucial role in the process of domestication from wild to cultivated fruit trees. However, the molecular mechanisms underlying fruit taste domestication still remain unclear. It is also unclear whether taste improvement is mainly determined by positive selection of advantageous traits such as sweetness or negative selection of disadvantageous trait such as acidity. Chinese jujube, domesticated from the wild jujube, is an economically important fruit tree crop in China. In this study, we sequenced and assembled the genome of a dry jujube and analyzed the genetic relationship between cultivated and wild jujubes through genome resequencing. Key genes involved in the acid and sugar metabolism were identified in the selective sweep regions. This finding suggested an important domestication pattern in fruit taste and also provided insights into the fruit molecular breeding and improvement.
  Jujube (Ziziphus jujuba Mill.) belongs to the Rhamnaceae family and is a popular fruit tree species with immense economic and nutritional value. Here, we report a draft genome of the dry jujube cultivar 'Junzao' and the genome resequencing of 31 geographically diverse accessions of cultivated and wild jujubes (Ziziphus jujuba var. spinosa). Comparative analysis revealed that the genome of 'Dongzao', a fresh jujube, was ~86.5 Mb larger than that of the 'Junzao', partially due to the recent insertions of transposable elements in the 'Dongzao' genome. We constructed eight proto-chromosomes of the common ancestor of Rhamnaceae and Rosaceae, two sister families in the order Rosales, and elucidated the evolutionary processes that have shaped the genome structures of modern jujubes. Population structure analysis revealed the complex genetic background of jujubes resulting from extensive hybridizations between jujube and its wild relatives. Notably, several key genes that control fruit organic acid metabolism and sugar content were identified in the selective sweep regions. We also identified S-locus genes controlling gametophytic self-incompatibility and investigated haplotype patterns of the S locus in the jujube genomes, which would provide a guideline for parent selection for jujube crossbreeding. This study provides valuable genomic resources for jujube improvement, and offers insights into jujube genome evolution and its population structure and domestication.
Author Huang, Jian
Li, Xingang
Yin, Xiao
Zhang, Chunmei
Gao, Lizhi
Li, Ruiqiang
Fei, Zhangjun
Wan, KangKang
Pang, Xiaoming
Bai, Yang
Zhang, Zhong
Sun, Xiaoqing
Zhao, Xing
Zhang, Jinbo
AuthorAffiliation 2 Center for Jujube Engineering and Technology of State Forestry Administration, Northwest A&F University, Yangling, China
4 Boyce Thompson Institute, Cornell University, Ithaca, New York, United States of America
5 College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China
1 College of Forestry, Northwest A&F University, Yangling, China
The University of North Carolina at Chapel Hill, UNITED STATES
6 Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species in Southwest China, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China
3 Novogene Bioinformatics Institute, Beijing, China
AuthorAffiliation_xml – name: 3 Novogene Bioinformatics Institute, Beijing, China
– name: 1 College of Forestry, Northwest A&F University, Yangling, China
– name: 5 College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China
– name: The University of North Carolina at Chapel Hill, UNITED STATES
– name: 6 Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species in Southwest China, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China
– name: 2 Center for Jujube Engineering and Technology of State Forestry Administration, Northwest A&F University, Yangling, China
– name: 4 Boyce Thompson Institute, Cornell University, Ithaca, New York, United States of America
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  orcidid: 0000-0001-7945-5355
  surname: Huang
  fullname: Huang, Jian
– sequence: 2
  givenname: Chunmei
  surname: Zhang
  fullname: Zhang, Chunmei
– sequence: 3
  givenname: Xing
  surname: Zhao
  fullname: Zhao, Xing
– sequence: 4
  givenname: Zhangjun
  orcidid: 0000-0001-9684-1450
  surname: Fei
  fullname: Fei, Zhangjun
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  givenname: KangKang
  surname: Wan
  fullname: Wan, KangKang
– sequence: 6
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  fullname: Zhang, Zhong
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  fullname: Pang, Xiaoming
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  surname: Sun
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– sequence: 14
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  orcidid: 0000-0001-7945-5355
  surname: Li
  fullname: Li, Xingang
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28005948$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Huang J, Zhang C, Zhao X, Fei Z, Wan K, Zhang Z, et al. (2016) The Jujube Genome Provides Insights into Genome Evolution and the Domestication of Sweetness/Acidity Taste in Fruit Trees. PLoS Genet 12(12): e1006433. doi:10.1371/journal.pgen.1006433
2016 Huang et al 2016 Huang et al
2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Huang J, Zhang C, Zhao X, Fei Z, Wan K, Zhang Z, et al. (2016) The Jujube Genome Provides Insights into Genome Evolution and the Domestication of Sweetness/Acidity Taste in Fruit Trees. PLoS Genet 12(12): e1006433. doi:10.1371/journal.pgen.1006433
Copyright_xml – notice: 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Huang J, Zhang C, Zhao X, Fei Z, Wan K, Zhang Z, et al. (2016) The Jujube Genome Provides Insights into Genome Evolution and the Domestication of Sweetness/Acidity Taste in Fruit Trees. PLoS Genet 12(12): e1006433. doi:10.1371/journal.pgen.1006433
– notice: 2016 Huang et al 2016 Huang et al
– notice: 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Huang J, Zhang C, Zhao X, Fei Z, Wan K, Zhang Z, et al. (2016) The Jujube Genome Provides Insights into Genome Evolution and the Domestication of Sweetness/Acidity Taste in Fruit Trees. PLoS Genet 12(12): e1006433. doi:10.1371/journal.pgen.1006433
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Conceptualization: XL JH RL.Data curation: XL.Formal analysis: JZ XZ ZF JH CZ ZZ.Investigation: XL JH CZ ZZ XY YB.Methodology: JH CZ JZ XZ XS.Project administration: XL JH.Resources: XL XP JH CZ ZZ XY LG.Software: JZ XZ KW XS RL.Supervision: XL.Visualization: JH CZ ZF XL YB.Writing – original draft: JH XL JZ.Writing – review & editing: JH ZF CZ XL.
The authors have declared that no competing interests exist.
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Snippet Jujube (Ziziphus jujuba Mill.) belongs to the Rhamnaceae family and is a popular fruit tree species with immense economic and nutritional value. Here, we...
Jujube ( Ziziphus jujuba Mill.) belongs to the Rhamnaceae family and is a popular fruit tree species with immense economic and nutritional value. Here, we...
  Jujube (Ziziphus jujuba Mill.) belongs to the Rhamnaceae family and is a popular fruit tree species with immense economic and nutritional value. Here, we...
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StartPage e1006433
SubjectTerms Acids
Bioinformatics
Biology and Life Sciences
Chromosome Mapping
Colleges & universities
Domestication
Engineering
Evolution
Evolution, Molecular
Fruit - genetics
Fruits
Genome, Plant
Genomes
Genomics
Germplasm
Metabolism
Microsatellite Repeats - genetics
Molecular Sequence Annotation
Phylogeny
Research and Analysis Methods
Rhamnaceae
Rosaceae
Rosales
Sequence Alignment
Taste - genetics
Trees
Ziziphus
Ziziphus - genetics
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Title The Jujube Genome Provides Insights into Genome Evolution and the Domestication of Sweetness/Acidity Taste in Fruit Trees
URI https://www.ncbi.nlm.nih.gov/pubmed/28005948
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https://doaj.org/article/fde3d51aed6247c6aac0523b47d2cd09
http://dx.doi.org/10.1371/journal.pgen.1006433
Volume 12
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