Integration of pluripotency pathways regulates stem cell maintenance in the Arabidopsis shoot meristem

Integration of pluripotency pathways regulates stem cell maintenance in the Arabidopsis shoot meristem
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多能性途径的整合调节拟南芥芽分生组织中干细胞的维持

DOI:
10.1073/pnas.2015248117
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发表时间:
2020
期刊:
Proceedings of the National Academy of Sciences
影响因子:
--
通讯作者:
Xian Sheng Zhang
Xian Sheng Zhang
中科院分区:
其他
文献类型:
--
作者:
Ying Hua Su;Chao Zhou;Ying Ju Li;Yang Yu;Li Ping Tang;Wen Jie Zhang;Wang Jin Song Yao;Rongfeng Huang;Thomas Laux;Xian Sheng Zhang

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意义:多能干细胞在动物和植物发育中都是至关重要的。与高等动物不同,植物有独特的胚胎后发育,依靠茎和根分生组织不断产生器官。在茎分生组织中,最外层的干细胞分裂为所有的茎结构提供细胞。这些分生组织细胞是如何受到严格控制的,引起了激烈的研究。在拟南芥中,遗传和分子分析已经确定关键转录因子WUSCHEL(WUS)和SHOTMERISTEMLESS(STM)是茎分生组织多能性的主要调节因子。在这里,这些结果提供了确凿的证据,表明这两个多能因子WUS和STM是如何协同严格控制植物中的茎分生组织细胞的。在茎分生组织中,WUSCHEL(WUS)和STM(STM)这两个时空表达模式重叠的转录因子对于维持干细胞处于未分化状态是必不可少的。尽管这两条途径很重要,但目前还不清楚这两条途径是如何整合在一起来协调干细胞发展的。在这里,我们证明了WUS和STM通路在拟南芥中通过WUS和STM蛋白之间的直接相互作用而收敛。STM与CLAVATA3(CLV3)启动子结合,并通过WUS-STM相互作用增强WUS与同一启动子的结合。在CLV3启动子的两个位置上,WUS和STM的异二聚化和同时结合都是调节CLV3表达所必需的,这反过来又维持了干细胞的恒定数量。此外,STM的表达依赖于WUS,这种WUS激活的STM表达增强了WUS介导的干细胞活性。我们的数据为理解茎分生组织中的空间表达模式如何转化为干细胞内稳态的调节单位提供了一个框架。
Significance Pluripotent stem cells are critical in both animal and plant development. Unlike higher animals, plants have unique postembryonic development, which continuously produce organs depending on shoot and root meristems. In the shoot meristem, division of the stem cells in the outermost layers provides the cells for all shoot structures. How those meristem cells are tightly controlled attracted intense studies. Genetic and molecular analyses in Arabidopsis have identified the key transcription factors WUSCHEL (WUS) and SHOOTMERISTEMLESS (STM) as the major regulators of pluripotency in the shoot meristem. Here, the results provide solid evidence showing how those two pluripotency factors WUS and STM coordinate to control shoot meristem cells strictly in plants. In the shoot meristem, both WUSCHEL (WUS) and SHOOT MERISTEMLESS (STM), two transcription factors with overlapping spatiotemporal expression patterns, are essential for maintaining stem cells in an undifferentiated state. Despite their importance, it remains unclear how these two pathways are integrated to coordinate stem cell development. Here, we show that the WUS and STM pathways in Arabidopsis thaliana converge through direct interaction between the WUS and STM proteins. STM binds to the promoter of CLAVATA3 (CLV3) and enhances the binding of WUS to the same promoter through the WUS–STM interaction. Both the heterodimerization and simultaneous binding of WUS and STM at two sites on the CLV3 promoter are required to regulate CLV3 expression, which in turn maintains a constant number of stem cells. Furthermore, the expression of STM depends on WUS, and this WUS-activated STM expression enhances the WUS-mediated stem cell activity. Our data provide a framework for understanding how spatial expression patterns within the shoot meristem are translated into regulatory units of stem cell homeostasis.