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iScience:拟南芥剪切体亚基JANUS通过转录调控WOX2和PIN7作用于早期胚胎模式建成

已有 784 次阅读 2019-10-4 19:09 |个人分类:每日摘要|系统分类:论文交流

Arabidopsis JANUS Regulates Embryonic Pattern Formation through Pol II-Mediated Transcription of WOX2 and PIN7


First author: Feng Xiong; Affiliations: Shandong Agricultural University (山东农业大学)Tai'an, China

Corresponding author: Sha Li


Embryonic pattern formation relies on positional coordination of cell division and specification. Early axis formation during Arabidopsis embryogenesis requires WUSCHEL RELATED HOMEOBOX (WOX)-mediated transcription activation and PIN-FORMED7 (PIN7)-mediated auxin asymmetry. How these events are regulated is obscure. We report that Arabidopsis JANUS, a putative subunit of spliceosome, is essential for embryonic pattern formation. Significantly reduced transcription but not mRNA processing of WOX2 and PIN7 in janus suggested its role in transcriptional regulation. JANUS interacts with RNA polymerase II (Pol II) through a region outside of its spliceosome-association domain. We further show that Pol II mediates the transcription of WOX2 and PIN7 in a JANUS-dependent way and is essential for embryonic pattern formation. These findings reveal that JANUS recruits Pol II for the activation of two parallel pathways to ensure proper pattern formation during embryogenesis.


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胚胎模式建成依赖于细胞分裂和特化的位置协调。拟南芥胚胎发生早期轴的形成需要WOX介导的转录激活以及PIN7介导的生长素不对称分布。然而,这些事件具体是由哪些分子机制调控的还不清楚。本文中,作者报道了拟南芥中一个剪切体亚基JANUS作用于胚胎模式建成。janus突变体中WOX2PIN7基因的转录水平显著降低,但mRNA加工没有显著变化,说明JANUS通过转录调控起作用。JANUS能够通过其剪切体相关结构域外的一个区域与RNA聚合酶Pol II互作。作者进一步的研究显示通过JANUS依赖型的方式介导了WOX2PIN7基因的转录,并且对于拟南芥胚胎模式的建成非常重要。本文的发现揭示了JANUS通过招募Pol II来激活两个平行的通路来保证胚胎发生过程中正确的模式建成。



Development of a specific body plan during embryogenesis requires precise cell fate determination based on the position of cells along the embryo axes. In Arabidopsis, the crucial cell types are established extremely early during embryogenesis as reflected by the stereotypic sequence of oriented cell divisions (Lau et al., 2012; ten Hove et al., 2015). Two pathways have been linked to the establishment of apical-basal axis and cell specification after zygotic division. One involves the transcription factors WUSCHEL RELATED HOMEOBOX2 (WOX2), WOX8, and WOX9, whereas the other depends on auxin, whose asymmetry is maintained by auxin efflux carrier PIN-FORMED7 (PIN7) (Lau et al., 2012). WOX2 and WOX8 are initially co-expressed in the zygote (Haecker et al., 2004). After zygotic division, WOX2 and WOX8 are restricted to the apical and basal cell lineage to control the following cell specification, respectively (Breuninger et al., 2008; Haecker et al., 2004). PIN7 is polarly localized to the apical plasma membrane (PM) of the basal cell, where it provides maternal auxin to the apical cell (Friml et al., 2003; Robert et al., 2018). The polar distribution of PIN7 ensures auxin maximum in the apical cell, which generates the proembryo and all apical structures of the plant. Functional loss of WOX2 or PIN7 compromised the formation of apical-basal axis during early embryogenesis. However, their defects at early embryonic pattern formation are later recovered (Friml et al., 2003; Robert et al., 2018). Whether these two pathways play redundant roles in embryogenesis and how their specific expression is controlled are unclear.



胚胎发生过程中特定体轴的形成需要精确的细胞命运决定,而这依赖于沿着胚轴方向细胞位置的确定。在拟南芥中,关键的细胞类型在极早期胚胎发生时就已经确定了,这个时候的细胞已经开始了定向分裂。在合子分裂后,两个通路一起作用于顶-基轴的建立及细胞特化。其中一条通路涉及了WOX2、WOX8及WOX9,而另一条通路主要依赖于生长素,其中PIN7作用于生长素的不对称性。WOX2WOX8在合子中共表达,在合子分裂后,分别在顶细胞系和基细胞系中特异表达,控制随后的细胞特化。PIN7蛋白极性定位于基细胞的顶部质膜,为顶细胞提供来自母本的生长素。PIN7的极性分化保证了生长素在顶细胞中达到最大值,从而形成原胚以及植物所有的顶部结构。WOX2或者PIN7的功能缺失会导致早期胚胎发生过程中顶-基轴建立的缺陷。然而,这种缺陷在后来的胚胎发生过程中会逐渐被恢复。胚胎发生过程中这两个通路是否存在功能冗余以及这两个基因的表达调控机制还不清楚。



RNA polymerase II (Pol II) plays a pivotal role in regulating gene expression (Thomas and Chiang, 2006). Pol II in Arabidopsis consists of 12 core subunits (Ream et al., 2009), in which Nuclear RNA Polymerase B1 (NRPB1) and NRPB2 interact to form the catalytic center for RNA synthesis, whereas other subunits play structural and regulatory roles in transcription initiation, elongation, termination, or RNA processing (Cramer et al., 2008; Werner and Grohmann, 2011). Functional studies of genes encoding for Pol II subunits suggested its role in embryogenesis such that no homozygous mutants could be obtained for functional loss of NRPB2, as well as that of NRPB9 and NRPB11, genes encoding for the noncatalytic subunits of Pol II (Onodera et al., 2008; Ream et al., 2009; Tan et al., 2012). However, whether and how functional loss of Pol II affects embryogenesis is unclear.



RNA聚合酶Pol II在调控基因表达方面发挥重要作用。拟南芥中的Pol II由12个核心亚基组成,其中NRPB1和NRPB2互作形成RNA合成的催化中心,而其他亚基则在转录起始、延伸、终止或者RNA加工过程中发挥结构或调控作用。对于Pol II亚基编码基因的功能研究显示其作用于胚胎发生,因此不能获得NRPB2功能缺失的纯合突变体,另外两个非核心亚基编码基因NRPB9NRPB11同样也不能获得能缺失的纯合突变体。然而,Pol II是否以及如何影响胚胎发生的还不清楚。



Spliceosomes are large RNA-protein complexes mainly involved in pre-mRNA splicing. Nevertheless, subunits of spliceosomes also participate in many other processes, including mRNA export (Howard and Sanford, 2015; Muller-McNicoll et al., 2016), the maintenance of genome stability (Li and Manley, 2005; Xiao et al., 2007), and microRNA processing (Ben Chaabane et al., 2013; Wu et al., 2010). Interestingly, reports both in metazoans and in plants showed that a subunit of spliceosome, Serine/arginine-rich splicing factor 35 (SC35), interacts with a Pol II subunit and is required for the transcription of genes, in addition to its role in pre-mRNA splicing (Lin et al., 2008; Yan et al., 2017). A role of the spliceosome subunit in regulating Pol II-mediated transcription was proposed (Yan et al., 2017).



剪切体是比较大的RNA蛋白复合物,主要参与mRNA前体的剪切。尽管如此,剪切体的亚基同样参与许多其他的生物学进程,包括mRNA的输出、基因组稳定性的维持以及microRNA的加工。有趣的是,在后生动物和植物的报道中均表明一个剪切体的亚基富含丝氨酸/精氨酸的剪接因子SC35可以与一个Pol II亚基互作,并且除了作用于mRNA前体剪切外,其还能作用于基因的转录。因此,Yan提出了剪切体亚基可能还参与了Pol II介导的转录调控。



In this study, we report that the Arabidopsis homolog of human SPLICEOSOME-ASSOCIATED PROTEIN 49 (SAP49) and yeast Hsh49p, a subunit of spliceosome, is essential for pattern formation during early embryogenesis. We named it JANUS as it represents the god of new beginnings in ancient Rome and associates with the first steps of a journey. Functional loss of JANUS resulted in complete embryo lethality due to abnormal cell division immediately after the first zygotic division. The specific expression of PIN7 was disrupted in janus, resulting in defective auxin signaling. On the other hand, WOX2 was also transcriptionally downregulated in janus. Consistently, the disruption of both WOX2- and PIN7-dependent pathways resembled pattern formation defects of janus during early embryogenesis. We further showed that JANUS interacts with Pol II subunits independent of its role as a splicing factor and is required for Pol II-dependent transcription of WOX2 and PIN7. Indeed, functional loss of Pol II subunits mimicked embryonic defects of janus. Taken together, our findings demonstrate that JANUS recruits Pol II to transcriptionally activate WOX2- and PIN7-mediated pathways for pattern formation during early embryogenesis.



本文中,作者报道了拟南芥中一个剪切体亚基、人类剪切体相关蛋白SAP49和酵母Hsh49p的同源蛋白对于早期的胚胎模式建成至关重要。作者将其命名为JANUS,寓意古罗马的新起点之神,旅程的起点。JANUS的功能缺失由于合子第一次分裂后的细胞分裂异常,导致胚胎百分百致死。janus突变体中PIN7基因的表达受到破坏,导致生长素信号转导的缺陷。另外,janus突变体中WOX2基因的表达下调。一致的是,WOX2PIN7依赖通路的破环会导致janus突变体类似的早期胚胎发育缺陷表型。作者进一步的研究显示JANUS能够与Pol II亚基互作,并且独立于其作为剪切因子的作用,并且对于Pol II依赖型的WOX2PIN7转录调控是必须的。确实,Pol II亚基的功能缺失导致的胚胎发生缺陷类似于janus突变体。综上,本文的研究揭示了JANUS招募Pol II来转录激活WOX2PIN7介导的通路作用于早期胚胎发生中的模式建成。



通讯:李厦 (http://life.sdau.edu.cn/2013/0514/c2453a27262/page.htm)


个人简介:2005年,德国科隆大学,硕士;2014年,山东农业大学,博士。


研究方向:1. 蛋白质棕榈酰化:通过反向遗传学对执行棕榈酰化这种修饰的PAT家族进行系统分析;2. 根毛的生长调控机制:探讨小G蛋白ROP以及乙烯在根毛生长中的作用机理;3. 植物有性生殖:揭示有性生殖过程中的细胞信号传导及细胞交流。



doi: https://doi.org/10.1016/j.isci.2019.09.004


Journal: iScience

Published date: September 09, 2019


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http://blog.sciencenet.cn/blog-3158122-1200597.html

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