Transcriptome analysis of gynoecium morphogenesis uncovers the chronology of gene regulatory network activity

Transcriptome analysis of gynoecium morphogenesis uncovers the chronology of gene regulatory network activity
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DOI:
10.1093/plphys/kiaa090
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发表时间:
2021-03-01
期刊:
影响因子:
7.4
通讯作者:
Becker, Annette
Becker, Annette
中科院分区:
生物学1区
文献类型:
--
作者:
Kivivirta, Kimmo, I;Herbert, Denise;Becker, Annette

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雌蕊是开花植物形成的最复杂的器官。它包裹胚珠,为花粉接触和自交不亲和反应提供表面,允许花粉管生长,并在受精后发育成果实。因此,雌蕊群形态发生的调控是复杂的,这一过程的适当时机在一定程度上决定了生殖的成功。然而,尽管已经确定了许多调控基因的特征,但对雌核发育的全球控制知之甚少。在这里,我们使用激光显微解剖的拟南芥四个发育阶段的雌蕊组织来描述基因表达的动态变化。我们提供了雌蕊群形态发生过程中全球表达动态的高分辨率图谱,并将其与雌蕊群相互作用组联系起来。我们揭示了一组基因在形态发生中一起作用的早期和其他作用的晚期。共表达基因的聚集使得能够比较叶片、茎尖和雌蕊群的转录本,从而能够剖析共同和不同的调控因子。此外,我们的结果导致发现了具有转录因子活性的基因(B3LF1,-2,DOFLF1),当这些基因突变时,会导致雌蕊群扩张受损,这表明全球转录组分析揭示了未知的发育调控因子。我们的数据表明,编码高相互作用蛋白的基因,如SEPALLATA3、AGAMOUS和TOBLIST,在发育过程中均匀表达,但随着时间的推移切换相互作用单位,而阶段特有的蛋白质往往有较少的相互作用单位。我们的分析将特定的转录调控活性、蛋白质相互作用和潜在的代谢过程联系在一起,为雌蕊群发育提供了一个动态的网络模型。
The gynoecium is the most complex organ formed by the flowering plants. It encloses the ovules, provides a surface for pollen contact and self-incompatibility reactions, allows pollen tube growth, and, post fertilization, develops into the fruit. Consequently, the regulation of gynoecium morphogenesis is complex and appropriate timing of this process in part determines reproductive success. However, little is known about the global control of gynoecium development, even though many regulatory genes have been characterized. Here, we characterized dynamic gene expression changes using laser-microdissected gynoecium tissue from four developmental stages in Arabidopsis. We provide a high-resolution map of global expression dynamics during gynoecium morphogenesis and link these to the gynoecium interactome. We reveal groups of genes acting together early and others acting late in morphogenesis. Clustering of co-expressed genes enables comparisons between the leaf, shoot apex, and gynoecium transcriptomes, allowing the dissection of common and distinct regulators. Furthermore, our results lead to the discovery of genes with putative transcription factor activity (B3LF1, -2, DOFLF1), which, when mutated, lead to impaired gynoecium expansion, illustrating that global transcriptome analyses reveal yet unknown developmental regulators. Our data show that genes encoding highly interacting proteins, such as SEPALLATA3, AGAMOUS, and TOPLESS, are expressed evenly during development but switch interactors over time, whereas stage-specific proteins tend to have fewer interactors. Our analysis connects specific transcriptional regulator activities, protein interactions, and underlying metabolic processes, contributing toward a dynamic network model for gynoecium development.