Genomic architecture of biomass heterosis in Arabidopsis

Genomic architecture of biomass heterosis in Arabidopsis
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DOI:
10.1073/pnas.1705423114
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发表时间:
2017-07
期刊:
Proceedings of the National Academy of Sciences
影响因子:
--
通讯作者:
Mei Yang;Xuncheng Wang;Diqiu Ren;Hao Huang;Miqi Xu;Guangming He;X. Deng
Mei Yang;Xuncheng Wang;Diqiu Ren;Hao Huang;Miqi Xu;Guangming He;X. Deng
中科院分区:
其他
文献类型:
--
作者:
Mei Yang;Xuncheng Wang;Diqiu Ren;Hao Huang;Miqi Xu;Guangming He;X. Deng

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意义 杂种优势,即杂种相对于其亲本的表型优势,已在农业中广泛利用,以提高生物量和产量。尽管杂种优势在农业上具有重要意义,但其遗传成分仍不清楚。在这里,我们描述了未经过驯化的拟南芥杂种优势的基因组结构,并利用全基因组关联研究鉴定了数百个共同促进生物量杂种优势的遗传位点。对代表性杂种中候选基因的功能研究和转录组分析表明,杂种中涉及基本生物过程的优势基因的积累和刺激响应基因的抑制有助于拟南芥生物量杂种优势,从而为植物物种自然群体中杂种优势的遗传基础提供了全面的了解。杂种优势最常见的表现是与亲本相比,杂种的生长旺盛。研究自然群体中的基因组变异对于了解植物杂种优势的初始分子机制至关重要。在这里,我们描述了 200 个拟南芥杂种中与生物量杂种优势相关的基因组结构。杂种的全基因组杂合度对生物量杂种优势的贡献有限,没有位点在杂种中表现出明显的超优势效应。然而,杂种全基因组关联研究(GWAS)中发现的重要遗传位点的积累与更好亲本杂种优势(BPH)密切相关。生物量 BPH 的候选基因属于多种生物功能,包括细胞、代谢和发育过程以及刺激响应途径。重要的杂种优势候选者包括 WUSCHEL、ARGOS 和一些编码参与细胞周期调节的关键因子的基因。有趣的是,代表性拟南芥杂交组合的转录组分析表明,杂种优势候选基因在刺激响应途径中功能丰富,包括对生物和非生物刺激的反应以及免疫反应。此外,在具有高 BPH 的杂种中,刺激响应基因被抑制至低亲本水平,而在没有 BPH 的杂种中则表现出中等亲本表达模式。我们的研究揭示了用于理解拟南芥生物量杂种优势分子机制的基因组结构,其中参与代谢和细胞过程的基因的优良等位基因的积累改善了杂种的发育和生长,而刺激响应基因的整体抑制表达在正常条件下优先考虑杂种中的生长而不是对环境刺激的响应。
Significance Heterosis, the phenotypic superiority of a hybrid over its parents, has been extensively exploited in agriculture to improve biomass and yield. Despite its great agricultural importance, the genetic components underlying heterosis remain largely unclear. Here, we characterize the genomic architecture of heterosis in Arabidopsis that have not undergone domestication and identify hundreds of genetic loci that collectively contribute to biomass heterosis using genome-wide association studies. The functional investigation of candidate genes and transcriptomic analysis in representative hybrids suggest that the accumulation of superior genes involved in basic biological processes and the repression of stimulus-responsive genes in hybrids contribute to biomass heterosis in Arabidopsis, thus providing a comprehensive understanding of the genetic bases of heterosis in natural populations of plant species. Heterosis is most frequently manifested by the substantially increased vigorous growth of hybrids compared with their parents. Investigating genomic variations in natural populations is essential to understand the initial molecular mechanisms underlying heterosis in plants. Here, we characterized the genomic architecture associated with biomass heterosis in 200 Arabidopsis hybrids. The genome-wide heterozygosity of hybrids makes a limited contribution to biomass heterosis, and no locus shows an obvious overdominance effect in hybrids. However, the accumulation of significant genetic loci identified in genome-wide association studies (GWAS) in hybrids strongly correlates with better-parent heterosis (BPH). Candidate genes for biomass BPH fall into diverse biological functions, including cellular, metabolic, and developmental processes and stimulus-responsive pathways. Important heterosis candidates include WUSCHEL, ARGOS, and some genes that encode key factors involved in cell cycle regulation. Interestingly, transcriptomic analyses in representative Arabidopsis hybrid combinations reveal that heterosis candidate genes are functionally enriched in stimulus-responsive pathways, including responses to biotic and abiotic stimuli and immune responses. In addition, stimulus-responsive genes are repressed to low-parent levels in hybrids with high BPH, whereas middle-parent expression patterns are exhibited in hybrids with no BPH. Our study reveals a genomic architecture for understanding the molecular mechanisms of biomass heterosis in Arabidopsis, in which the accumulation of the superior alleles of genes involved in metabolic and cellular processes improve the development and growth of hybrids, whereas the overall repressed expression of stimulus-responsive genes prioritizes growth over responding to environmental stimuli in hybrids under normal conditions.