Comparison of genome-wide gene expression patterns in the seedlings of nascent allohexaploid wheats produced by two combinations of hybrids

Abstract

Allopolyploidization in plants is an important event that enhances heterosis and environmental adaptation. Common wheat, Triticum aestivum (AABBDD), which is an allohexaploid that evolved from an allopolyploidization event between T. turgidum (AABB) and Aegilops tauschii (DD), shows more growth vigor and wider adaptation than tetraploid wheats. To better understand the molecular basis for the heterosis of hexaploid wheat, we systematically analyzed the genomewide gene expression patterns of two combinations of newly hybridized triploids (ABD), their chromosome-doubled hexaploids (AABBDD), stable synthetic hexaploids (AABBDD) and natural hexaploids, in addition to their parents, T. turgidum (AABB) and Ae. tauschii (DD), using a microarray to reconstruct the events of allopolyploidization and genome stabilization. Overall comparisons of gene expression profiles showed that the newly generated hexaploids exhibited gene expression patterns similar to those of their maternal tetraploids, irrespective of hybrid combination. With successive generations, the gene expression profiles of nascent hexaploids became less similar to the maternal profiles, and belonged to a separate cluster from the natural hexaploids. Triploids revealed characteristic expression patterns, suggesting endosperm effects. In the newly hybridized triploids (ABD) of two independent synthetic lines, approximately onefifth of expressed genes displayed non-additive expression; the number of these genes decreased with polyploidization and genome stabilization. Approximately 20% of the non-additively expressed genes were transmitted across generations throughout allopolyploidization and successive self-pollinations, and 43 genes overlapped between the two combinations, indicating that shared gene expression patterns can be seen during allohexaploidization. Furthermore, four of these 43 genes were involved in starch and sucrose metabolism, suggesting that these metabolic events play key roles in the hybrid vigor of hexaploid wheat.

Cross‐kingdom transcriptomic trends in the evolution of hybrid gene expression

“…Current literature suggests that hybridization, rather than the increase in ploidy level, has a greater impact on post‐allopolyploidization gene expression patterns (Albertin et al, 2006; Chelaifa et al, 2010; Hegarty et al, 2005, 2006; Jung et al, 2015; Li et al, 2018; Wang et al, 2006). Our results are consistent with this view, as there are no clear differences in gene expression patterns between the allopolyploid and homoploid hybrid systems (Figures 2–5).…”

“…Also consistent is our result suggesting that hybridization, rather than change in ploidy level, is the major driver of hybrid expression patterns, as this mechanism is dependent on genome merger, but independent of an increase in ploidy. Data from studies on other allopolyploid and homoploid hybrid species including Senecio (Hegarty et al, 2005, 2006), Brassica (Albertin et al, 2006), Arabidopsis (Wang et al, 2006), Spartina (Chelaifa et al, 2010), wheat (Jung et al, 2015) and Cyprinidae fish (Li et al, 2018) have also suggested that genome merger has a greater effect on gene expression patterns than an increase in ploidy.…”

“…Arabidopsis (Wang et al, 2006), Spartina (Chelaifa et al, 2010), wheat (Jung et al, 2015) and Cyprinidae fish (Li et al, 2018) have also suggested that genome merger has a greater effect on gene expression patterns than an increase in ploidy.…”

The importance and prevalence of allopolyploidy in Aotearoa New Zealand

“…The suite of potential biological responses, both rapid and longer term, employed by the allopolyploid in response to genome shock have many potential manifestations, including genomic restructuring (Lim et al 2008;Wu et al 2015;Qin et al 2016;Wang et al 2018) and gene loss (Scannell et al 2006;Gordon et al 2009;Vallejo-Marín et al 2015). Although the impact of allopolyploidy is most often viewed through the lens of nuclear genomic studies, organellar genomes (Sloan et al 2018), small RNAs (Ha et al 2009;Jiao et al 2018) and the gene expression profiles of allopolyploid species (Yoo et al 2014;Jung et al 2015) are also affected. Extensive changes in allopolyploid gene expression ('transcriptome shock') are driven by the mixing of two dissimilar and poorly co-adapted sets of transcription factors and chromatin signatures (Cox et al 2014).…”