FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis

FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis
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FAR-RED ELONGATED HYPOCOTYL3 激活 SEPALLATA2 但抑制 CLAVATA3 以调节拟南芥分生组织的决定性和维持

DOI:
10.1073/pnas.1602960113
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发表时间:
2016-08-16
影响因子:
11.1
通讯作者:
Liu, Xigang
Liu, Xigang
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Li, Dongming;Fu, Xing;Liu, Xigang

文献摘要

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转录因子FAR-RED ELLONGATED HYPOCOTYL 3(FHY 3)在拟南芥的营养生长阶段起着多种作用,但在生殖生长阶段的功能尚不清楚。我们发现,FHY 3是所需的花分生组织的决定性和茎顶端分生组织的维护,主要是作为一个转录抑制因子。FHY 3介导光调控CLAVATA 3的表达以调控茎顶端分生组织中WUSCHEL的表达,并直接抑制CLAVATA 3,但激活SEPALLATA 2,以促进花分生组织的决定性。此外,FHY 3还可能与3个花特异性MADS结构域转录因子和4个基本的helix-loop-helix转录因子共同调控花的发育,从而在外部信号和内源信号之间起桥梁作用,协调植物的发育。植物分生组织负责所有植物组织和器官的产生。在这里,我们表明,转录因子(TF)FAR-RED ELONGATED HYPOCOTYL 3(FHY 3)在拟南芥的花分生组织(FM)的确定性和芽顶端分生组织的维持中起着重要的作用,除了其众所周知的多方面的作用,在植物的生长和发育在营养阶段。通过遗传分析,我们表明,WUSCHEL(WUS)和CLAVATA 3(CLV 3),在分生组织的建立和维护的两个核心球员,上位FHY 3。利用全基因组ChIP-seq和RNA-seq数据,我们在花中鉴定了数百个FHY 3靶基因,发现FHY 3在花发育中主要作为转录抑制因子,而在幼苗中则是转录激活因子。结合基序富集分析表明,FHY 3可能与三个花特异性MADS结构域TF和四个基本的螺旋-环-螺旋TF参与光形态建成共调节花的发育。我们进一步证明CLV 3、SEPALLATA 1(SEP 1)和SEP 2是FHY 3靶基因。在茎尖分生组织中,FHY 3直接抑制CLV 3,从而调节WUS以维持干细胞库。有趣的是,CLV 3的表达在光处理前后在fhy 3和光敏色素B突变体中没有显著变化,表明FHY 3和光敏色素B参与了光调节的分生组织活性。在FM中,FHY 3直接抑制CLV 3,但激活SEP 2,最终促进FM确定性。两者合计,我们的研究结果揭示了见解分生组织的维护和确定性的机制,并说明了如何在不同的器官和发育阶段的一个TF的作用可能有所不同。
Significance The transcription factor FAR-RED ELONGATED HYPOCOTYL3 (FHY3) is known to play multiple roles at the vegetative stage in Arabidopsis, but its functions in reproductive stage are unclear. We find that FHY3 is required for floral meristem determinacy and shoot apical meristem maintenance by mainly acting as a transcriptional repressor. FHY3 mediates light-regulated CLAVATA3 expression to regulate WUSCHEL expression in shoot apical meristem and directly represses CLAVATA3, but activates SEPALLATA2, to promote floral meristem determinacy. Furthermore, FHY3 may coregulate flower development with three flower-specific MADS-domain transcription factors and four basic helix–loop–helix transcription factors that are involved in photomorphogenesis, and thus may act as a bridge molecule in the cross-talk between external signals and endogenous cues to coordinate plant development. Plant meristems are responsible for the generation of all plant tissues and organs. Here we show that the transcription factor (TF) FAR-RED ELONGATED HYPOCOTYL3 (FHY3) plays an important role in both floral meristem (FM) determinacy and shoot apical meristem maintenance in Arabidopsis, in addition to its well-known multifaceted roles in plant growth and development during the vegetative stage. Through genetic analyses, we show that WUSCHEL (WUS) and CLAVATA3 (CLV3), two central players in the establishment and maintenance of meristems, are epistatic to FHY3. Using genome-wide ChIP-seq and RNA-seq data, we identify hundreds of FHY3 target genes in flowers and find that FHY3 mainly acts as a transcriptional repressor in flower development, in contrast to its transcriptional activator role in seedlings. Binding motif-enrichment analyses indicate that FHY3 may coregulate flower development with three flower-specific MADS-domain TFs and four basic helix–loop–helix TFs that are involved in photomorphogenesis. We further demonstrate that CLV3, SEPALLATA1 (SEP1), and SEP2 are FHY3 target genes. In shoot apical meristem, FHY3 directly represses CLV3, which consequently regulates WUS to maintain the stem cell pool. Intriguingly, CLV3 expression did not change significantly in fhy3 and phytochrome B mutants before and after light treatment, indicating that FHY3 and phytochrome B are involved in light-regulated meristem activity. In FM, FHY3 directly represses CLV3, but activates SEP2, to ultimately promote FM determinacy. Taken together, our results reveal insights into the mechanisms of meristem maintenance and determinacy, and illustrate how the roles of a single TF may vary in different organs and developmental stages.