Transcriptional Aneuploidy Responses of Brassica rapa-oleracea Monosomic Alien Addition Lines (MAALs) Derived From Natural Allopolyploid B. napus.

Zhu Bin,Huo Dongao,Li Zaiyun,Ge Xianhong,Cai Bowei,Pan Qi,Zeng Pan

doi:10.3389/fgene.2019.00067

Zhu Bin, Huo Dongao + Show 5 more

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https://doi.org/10.3389/fgene.2019.00067

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Abstract

Establishing the whole set of aneuploids, for one naturally evolved allopolyploid species, provides a unique opportunity to elucidate the transcriptomic response of the constituent subgenomes to serial aneuploidy. Previously, the whole set of monosomic alien addition lines (MAALs, C1-C9) with each of the nine C subgenome chromosomes, added to the extracted A subgenome, was developed in the context of the allotetraploid Brassica napus donor “Oro,” after the restitution of the ancestral B. rapa (RBR Oro) was realized. Herein, transcriptomic analysis using high-throughput technology was conducted to detect gene expression alterations in these MAALs and RBR. Compared to diploid RBR, the genes of all of the MAALs showed various degrees of dysregulated expressions that resulted from cis effects and more prevailing trans effects. In addition, the trans-effect on gene expression in MAALs increased with higher levels of homology between the recipient A subgenome and additional C subgenome chromosomes, instead of gene numbers of extra chromosomes. A total of 10 trans-effect dysregulated genes, among all pairwise comparisons, were mainly involved in the function of transporter activity. Furthermore, highly expressed genes were more prone to downregulation and vice-versa, suggesting a common trend for transcriptional pattern responses to aneuploidy. These results provided a comprehensive insight of the impact of gene expression of individual chromosomes, in one subgenome, on another intact subgenome for one allopolyploid with a long evolutionary history.

Highlights

Since monosomic alien addition line (MAAL) and restituted B. rapa (RBR) Oro were derived from one natural B. napus cultivar, the clean reads for all of the samples were aligned to the B. napus reference genome (Chalhoub et al, 2014)
Compared to RBR Oro, C1 presented a higher number of downregulated genes (1,895 Differentially Expressed Genes (DEGs) vs. 1,661 DEGs) (χ 2 test, p < 0.01), which indicated that the chromosomes of the A subgenome exhibit downregulated gene expression
Numerous studies demonstrated that dysregulated genes in aneuploidy are restricted to altered chromosome and disomic chromosomes (Huettel et al, 2008; Makarevitch and Harris, 2010; Letourneau et al, 2014; Zhu et al, 2015, 2018; Zhang et al, 2017), suggesting that this dysregulation in gene expression may be a collective transcriptional response to aneuploidy (Sheltzer et al, 2012)

Summary

Introduction

As a deviation from the normal genome, by either gaining or losing entire chromosomes or chromosomal segments, aneuploidy disrupts the genome balance, which generally results in profoundly and severely impaired phenotypes (Antonarakis et al, 2004; Birchler and Veitia, 2007; Huettel et al, 2008; Henry et al, 2010; Siegel and Amon, 2012; Zhu et al, 2015). Studies on aneuploids in Drosophila and plants showed that changes in the gene expression levels were observed along altered copy numbers (cis-effects) as well as in unaltered disomic chromosomes (trans-effects) (Guo and Birchler, 1994; Birchler and Veitia, 2007; Huettel et al, 2008; Malone et al, 2012; Zhu et al, 2015, 2018; Zhang et al, 2017; Rey et al, 2018). Aneuploids exhibit a more severe degree of perturbation in gene expression than changes in ploidy (Birchler and Newton, 1981; Guo et al, 1996), indicating a disruption in the dosage-sensitive gene products (Birchler et al, 2001; Henry et al, 2006)

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