Review Article | Published:

Gene retention, fractionation and subgenome differences in polyploid plants

Nature Plantsvolume 4pages258268 (2018) | Download Citation

Abstract

All natural plant species are evolved from ancient polyploids. Polyloidization plays an important role in plant genome evolution, species divergence and crop domestication. We review how the pattern of polyploidy within the plant phylogenetic tree has engendered hypotheses involving mass extinctions, lag-times following polyploidy, and epochs of asexuality. Polyploidization has happened repeatedly in plant evolution and, we conclude, is important for crop domestication. Once duplicated, the effect of purifying selection on any one duplicated gene is relaxed, permitting duplicate gene and regulatory element loss (fractionation). We review the general topic of fractionation, and how some gene categories are retained more than others. Several explanations, including neofunctionalization, subfunctionalization and gene product dosage balance, have been shown to influence gene content over time. For allopolyploids, genetic differences between parental lines immediately manifest as subgenome dominance in the wide-hybrid, and persist and propagate for tens of millions of years. While epigenetic modifications are certainly involved in genome dominance, it has been difficult to determine which came first, the chromatin marks being measured or gene expression. Data support the conclusion that genome dominance and heterosis are antagonistic and mechanically entangled; both happen immediately in the synthetic wide-cross hybrid. Also operating in this hybrid are mechanisms of ‘paralogue interference’. We present a foundation model to explain gene expression and vigour in a wide hybrid/new allotetraploid. This Review concludes that some mechanisms operate immediately at the wide-hybrid, and other mechanisms begin their operations later. Direct interaction of new paralogous genes, as measured using high-resolution chromatin conformation capture, should inform future research and single cell transcriptome sequencing should help achieve specificity while studying gene sub- and neo-functionalization.

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Acknowledgements

The Chinese authors are supported by the National Program on Key Research Project (2016YFD0100307), the National Natural Science Foundation of China (NSFC grants 31630068 and 31722048), the Prospect of Shandong Seed Project (Shandong Government, 2015, reference no. 212), the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences, and the Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture, P.R. China. MF’s support is from the National Science Foundation, USA, Plant Genome Research Program grant IOS-1546825 to R. Mosher and team.

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  1. Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Key Laboratory of Biology and Genetic Improvement of Horticultural Crops of the Ministry of Agriculture, Sino-Dutch Joint Laboratory of Horticultural Genomics, Beijing, China

    • Feng Cheng
    • , Jian Wu
    • , Xu Cai
    • , Jianli Liang
    •  & Xiaowu Wang
  2. Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA

    • Michael Freeling
  3. Shandong Provincial Key Laboratory of Protected Vegetable Molecular Breeding, Shandong Shouguang Vegetable Seed Industry Group Co. Ltd., Shandong Province, China

    • Xiaowu Wang

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The authors declare no competing interests

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Correspondence to Michael Freeling or Xiaowu Wang.

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