Balanced Genome Triplication in Wheat Causes Premature Growth Arrest and an Upheaval of Genome-Wide Gene Regulation.

Xiaowan Gou,Huakun Zhang,Ruili Lv,Yan Sha,Tiansi Fu,Lei Gong,Changyi Wang,Bao Liu

doi:10.3389/fgene.2020.00687

Xiaowan Gou, Huakun Zhang + Show 6 more

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https://doi.org/10.3389/fgene.2020.00687

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Abstract

Polyploidy, or whole genome duplication (WGD), is a driving evolutionary force across the tree of life and has played a pervasive role in the evolution of the plant kingdom. It is generally believed that a major genetic attribute contributing to the success of polyploidy is increased gene and genome dosage. The evolution of polyploid wheat has lent support to this scenario. Wheat has evolved at three ploidal levels: diploidy, tetraploidy, and hexaploidy. Ample evidence testifies that the evolutionary success, be it with respect to evolvability, natural adaptability, or domestication has dramatically increased with each elevation of the ploidal levels. A long-standing question is what would be the outcome if a further elevation of ploidy is superimposed on hexaploid wheat? Here, we characterized a spontaneously occurring nonaploid wheat individual in selfed progenies of synthetic hexaploid wheat and compared it with its isogenic hexaploid siblings at the phenotypic, cytological, and genome-wide gene-expression levels. The nonaploid manifested severe defects in growth and development, albeit with a balanced triplication of the three wheat subgenomes. Transcriptomic profiling of the second leaf of nonaploid, taken at a stage when phenotypic abnormality was not yet discernible, already revealed significant dysregulation in global-scale gene expression with ca. 25.2% of the 49,436 expressed genes being differentially expressed genes (DEGs) at a twofold change cutoff relative to the hexaploid counterpart. Both up- and downregulated DEGs were identified in the nonaploid vs. hexaploid, including 457 genes showing qualitative alteration, i.e., silencing or activation. Impaired functionality at both cellular and organismal levels was inferred from gene ontology analysis of the DEGs. Homoeologous expression analysis of 9,574 sets of syntenic triads indicated that, compared with hexaploid, the proportions showing various homeologous expression patterns were highly conserved in the nonaploid although gene identity showed moderate reshuffling among some of the patterns in the nonaploid. Together, our results suggest hexaploidy is likely the upper limit of ploidy level in wheat; crossing this threshold incurs severe ploidy syndrome that is preceded by disruptive dysregulation of global gene expression.

Highlights

We found that the subgenomes of both nonaploid and hexaploid were preferentially clustered together based on overall subgenome-specific expression level similarities (Supplementary Figure S2), suggesting balanced genome triplication did not cause a general disruption of the evolved homoeologous expression patterns of hexaploid wheat
We found that the nonaploid individual maintained a stable somatic karyotype with no numerical or structural chromosomal variations detected in any of the 15 well-spread root-tip metaphase cells examined, suggesting mitosis was not impaired in the nonaploid with a balanced genome triplication
Large-scale alteration of transcriptional gene expression was detected in the nonaploid relative to its isogenic hexaploid siblings in leaf tissue before the manifestation of phenotypic abnormality, suggesting gene dysregulation precedes the phenotypic abnormality

Summary

Introduction

Polyploidy, or whole-genome duplication (WGD), is an important evolutionary force that has shaped the genomes of all higher plants and many animals (Van de Peer et al, 2009; Jiao et al, 2011; Paterson et al, 2012; Soltis and Soltis, 2012; Jiao and Paterson, 2014; Wendel, 2015; Schwager et al, 2017; Van de Peer et al, 2017; Blischak et al, 2018; Spoelhof et al, 2019). Myriad attributes characterize polyploidy relative to its diploid counterpart with genome-wide increase of DNA content and gene dosage being at the root. Interspecific hybridization is another major evolutionary force that facilitates adaptation and speciation primarily via new combinations of old parental genetic variants (Soltis and Soltis, 2009; Marques et al, 2019), but it may include immediate effects of genome shock (McClintock, 1984) that induce new genetic and epigenetic variations (Kashkush et al, 2002; Senerchia et al, 2015). Polyploidy in general and allopolyploidy in particular are often associated with enhanced organismal performance in growth, yield, fitness, and evolvability (Comai, 2005; Doyle et al, 2008; Wendel, 2015; Van de Peer et al, 2017)

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