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Research ArticleLARGE-SCALE BIOLOGY ARTICLE
Open Access

mRNA and Small RNA Transcriptomes Reveal Insights into Dynamic Homoeolog Regulation of Allopolyploid Heterosis in Nascent Hexaploid Wheat

Aili Li, Dengcai Liu, Jun Wu, Xubo Zhao, Ming Hao, Shuaifeng Geng, Jun Yan, Xiaoxue Jiang, Lianquan Zhang, Junyan Wu, Lingjie Yin, Rongzhi Zhang, Liang Wu, Youliang Zheng, Long Mao
Aili Li
National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China
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Dengcai Liu
Triticeae Research Institute, Sichuan Agricultural University, Chengdu, Sichuan 611130, China
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Jun Wu
Novogene Bioinformatics Institute, Beijing 100083, China
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Xubo Zhao
National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China
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Ming Hao
Triticeae Research Institute, Sichuan Agricultural University, Chengdu, Sichuan 611130, China
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Shuaifeng Geng
National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China
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Jun Yan
Novogene Bioinformatics Institute, Beijing 100083, China
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Xiaoxue Jiang
Novogene Bioinformatics Institute, Beijing 100083, China
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Lianquan Zhang
Triticeae Research Institute, Sichuan Agricultural University, Chengdu, Sichuan 611130, China
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Junyan Wu
National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China
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Lingjie Yin
National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China
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Rongzhi Zhang
National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China
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Liang Wu
National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China
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Youliang Zheng
Triticeae Research Institute, Sichuan Agricultural University, Chengdu, Sichuan 611130, China
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Long Mao
National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China
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  • For correspondence: maolong@caas.cn

Published May 2014. DOI: https://doi.org/10.1105/tpc.114.124388

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  • © 2014 American Society of Plant Biologists. All rights reserved.

Abstract

Nascent allohexaploid wheat may represent the initial genetic state of common wheat (Triticum aestivum), which arose as a hybrid between Triticum turgidum (AABB) and Aegilops tauschii (DD) and by chromosome doubling and outcompeted its parents in growth vigor and adaptability. To better understand the molecular basis for this success, we performed mRNA and small RNA transcriptome analyses in nascent allohexaploid wheat and its following generations, their progenitors, and the natural allohexaploid cultivar Chinese Spring, with the assistance of recently published A and D genome sequences. We found that nonadditively expressed protein-coding genes were rare but relevant to growth vigor. Moreover, a high proportion of protein-coding genes exhibited parental expression level dominance, with genes for which the total homoeolog expression level in the progeny was similar to that in T. turgidum potentially participating in development and those with similar expression to that in Ae. tauschii involved in adaptation. In addition, a high proportion of microRNAs showed nonadditive expression upon polyploidization, potentially leading to differential expression of important target genes. Furthermore, increased small interfering RNA density was observed for transposable element–associated D homoeologs in the allohexaploid progeny, which may account for biased repression of D homoeologs. Together, our data provide insights into small RNA–mediated dynamic homoeolog regulation mechanisms that may contribute to heterosis in nascent hexaploid wheat.

  • Glossary

    MPV
    mid-parent value
    ELD
    expression-level dominance
    miRNA
    microRNA
    siRNA
    small interfering RNA
    TE
    transposable element
    CS
    Chinese Spring
    DAF
    days after flowering
    SNP
    single nucleotide polymorphism
    RPKM
    reads per kilobase of exon model per million mapped base pairs
    GO
    Gene Ontology
    BH
    Benjamini-Hochberg
    FDR
    false discovery rate
    TAG
    TE-associated gene
    • Received February 20, 2014.
    • Revised March 28, 2014.
    • Accepted April 28, 2014.
    • Published May 16, 2014.

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    mRNA and Small RNA Transcriptomes Reveal Insights into Dynamic Homoeolog Regulation of Allopolyploid Heterosis in Nascent Hexaploid Wheat
    Aili Li, Dengcai Liu, Jun Wu, Xubo Zhao, Ming Hao, Shuaifeng Geng, Jun Yan, Xiaoxue Jiang, Lianquan Zhang, Junyan Wu, Lingjie Yin, Rongzhi Zhang, Liang Wu, Youliang Zheng, Long Mao
    The Plant Cell May 2014, 26 (5) 1878-1900; DOI: 10.1105/tpc.114.124388

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    mRNA and Small RNA Transcriptomes Reveal Insights into Dynamic Homoeolog Regulation of Allopolyploid Heterosis in Nascent Hexaploid Wheat
    Aili Li, Dengcai Liu, Jun Wu, Xubo Zhao, Ming Hao, Shuaifeng Geng, Jun Yan, Xiaoxue Jiang, Lianquan Zhang, Junyan Wu, Lingjie Yin, Rongzhi Zhang, Liang Wu, Youliang Zheng, Long Mao
    The Plant Cell May 2014, 26 (5) 1878-1900; DOI: 10.1105/tpc.114.124388
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    The Plant Cell Online: 26 (5)
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    • Cell Cycle–Dependent Regulation and Function of ARGONAUTE1 in Plants
    • Breaking Free: The Genomics of Allopolyploidy-Facilitated Niche Expansion in White Clover
    • Genome-Wide Association Studies Reveal the Genetic Basis of Ionomic Variation in Rice
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