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

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. Overall design: Examination of gene expression in 5 tetraploid Arabidopsis using mRNA-seq

多倍体在众多植物与部分动物类群中催生了进化与形态学上的新奇性状。然而，基因组剂量与基因组组成在基因表达变化中所扮演的角色，目前仍未得到充分阐释。本研究构建了一系列携带0至4份拟南芥（Arabidopsis thaliana）和沙拟南芥（Arabidopsis arenosa）基因组拷贝的人工重合成四倍体拟南芥，并探究了倍性与杂交性对基因表达的影响。等位基因表达可分为剂量依赖性（表达水平与基因组剂量呈正相关）与非剂量依赖性两类。本研究发现，大量剂量依赖性基因参与细胞周期、光合作用与代谢过程，而非剂量依赖性基因则显著富集于生物与非生物胁迫响应通路中。有趣的是，剂量依赖性基因多保留于动植物共有的古老生化通路中，而非剂量依赖性基因则多隶属于植物特异性通路。该结论通过基于拟南芥系统发生层级图谱的独立分析得到了验证。针对拟南芥基因座，剂量依赖性等位基因不含转座因子（Transposable Elements, TEs），且多与H3K9ac、H3K4me3及CG甲基化修饰相关；而非剂量依赖性等位基因则大多富集转座因子，且对应H3K27me1、H3K27me3与CHG（H为A、T或C）甲基化修饰。此外，在正反交异源四倍体中，非加性表达基因存在亲本起源效应，尤以沙拟南芥作为花粉供体时最为显著，该效应可引发代谢与形态学变化。综上，倍性、表观遗传修饰及质核互作共同塑造了多倍体中的基因表达多样性。剂量依赖性表达可维持生长与发育稳定性，而非剂量依赖性表达则可促进多倍体进化过程中部分同源基因间的功能分化（亚功能化和/或新功能化）。实验设计：采用mRNA测序（mRNA-seq）技术检测5组四倍体拟南芥的基因表达水平。