Genome-Wide Dosage-Dependent and -Independent Regulation Contributes to Gene Expression and Evolutionary Novelty in Plant Polyploids

Abstract

Polyploidy provides evolutionary and morphological novelties in many plants and some animals. However, the role of genome dosage and composition in gene expression changes remains poorly understood. Here, we generated a series of resynthesized Arabidopsis tetraploids that contain 0-4 copies of Arabidopsis thaliana and Arabidopsis arenosa genomes and investigated ploidy and hybridity effects on gene expression. Allelic expression can be defined as dosage dependent (expression levels correlate with genome dosages) or otherwise as dosage independent. Here, we show that many dosage-dependent genes contribute to cell cycle, photosynthesis, and metabolism, whereas dosage-independent genes are enriched in biotic and abiotic stress responses. Interestingly, dosage-dependent genes tend to be preserved in ancient biochemical pathways present in both plant and nonplant species, whereas many dosage-independent genes belong to plant-specific pathways. This is confirmed by an independent analysis using Arabidopsis phylostratigraphic map. For A. thaliana loci, the dosage-dependent alleles are devoid of TEs and tend to correlate with H3K9ac, H3K4me3, and CG methylation, whereas the majority of dosage-independent alleles are enriched with TEs and correspond to H3K27me1, H3K27me3, and CHG (H = A, T, or C) methylation. Furthermore, there is a parent-of-origin effect on nonadditively expressed genes in the reciprocal allotetraploids especially when A. arenosa is used as the pollen donor, leading to metabolic and morphological changes. Thus, ploidy, epigenetic modifications, and cytoplasmic-nuclear interactions shape gene expression diversity in polyploids. Dosage-dependent expression can maintain growth and developmental stability, whereas dosage-independent expression can facilitate functional divergence between homeologs (subfunctionalization and/or neofunctionalization) during polyploid evolution.

Global Analysis of Gene Expression in Response to Whole-Chromosome Aneuploidy in Hexaploid Wheat

“…After this step, we identified 995 nondifferentially expressed genes residing on chromosome 1A from the M1A versus CS, Tri1A versus CS, and T1A versus CS pairwise comparisons and 1,285 nondifferentially expressed genes residing on chromosome 2A from the M2A versus CS and Tri2A versus CS pairwise comparisons. Second, a correlation test (Pearson correlation coefficient) between the expression level and the scaled-up dosage variation for each gene was performed according to the method described (Shi et al, 2015). If the correlation coefficient was significant for a given gene (FDR-adjusted P , 0.05), then it was removed from the candidate gene list.…”

Histone Modifications Define Expression Bias of Homoeologous Genomes in Allotetraploid Cotton

“…Polyploidy may induce epigenetic modifications of homeologous chromosomes to reprogram gene expression and developmental patterns of allopolyploids (Song and Chen, 2015), leading to genome-wide dosage-dependent and independent gene expression novelty (Shi et al, 2015). Histone marks such as H3K4me3 are known to correlate with gene expression diversity between species and in Arabidopsis allopolyploids (Ha et al, 2011;Shi et al, 2015).…”

Coordinated Functional Divergence of Genes after Genome Duplication in Arabidopsis thaliana

“…A range of phenotypic and genotypic effects might explain the relative success of polyploids (Van de Peer et al, 2017). It has been observed that polyploidy can have a direct influence on the plant phenotype, leading, for instance, to bigger flowers and/or increased stature (Chen, 2010;Gross and Schiestl, 2015), as well as on the plant genotype, leading to genomic rearrangements and gene expression changes (Adams and Wendel, 2005;Chen, 2007;Buggs et al, 2011;Chester et al, 2012;Shi et al, 2015).…”