Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

First author: Mark Greenwood; Affiliations: University of Cambridge (剑桥大学): Cambridge, UK

Corresponding author: James C. W. Locke

Individual plant cells have a genetic circuit, the circadian clock, that times key processes to the day-night cycle. These clocks are aligned to the day-night cycle by multiple environmental signals that vary across the plant. How does the plant integrate clock rhythms, both within and between organs, to ensure coordinated timing? To address this question, we examined the clock at the sub-tissue level across Arabidopsis thaliana seedlings under multiple environmental conditions and genetic backgrounds. Our results show that the clock runs at different speeds (periods) in each organ, which causes the clock to peak at different times across the plant in both constant environmental conditions and light-dark (LD) cycles. Closer examination reveals that spatial waves of clock gene expression propagate both within and between organs. Using a combination of modeling and experiment, we reveal that these spatial waves are the result of the period differences between organs and local coupling, rather than long-distance signaling. With further experiments we show that the endogenous period differences, and thus the spatial waves, can be generated by the organ specificity of inputs into the clock. We demonstrate this by modulating periods using light and metabolic signals, as well as with genetic perturbations. Our results reveal that plant clocks can be set locally by organ-specific inputs but coordinated globally via spatial waves of clock gene expression.

单个植物细胞都具有一个叫做生物钟的遗传回路，能够根据日夜周期调节细胞内生物学进程的节律。这些生物钟通过多个环境信号与日夜周期进行匹配，不同植物物种利用的环境信号各不相同。至于植物如何整合器官内和器官间的生物钟节律以保证整个植株的正常生长发育还不清楚。为了解决这个问题，本文作者对多个遗传背景的拟南芥实生苗在多个环境条件下的亚组织水平上的生物钟进行了研究。本文的研究结果显示生物钟在不同的器官间是不一致的，这导致了无论是在恒定的环境条件下，还是在光照/黑暗周期循环条件下，植物不同器官生物钟出现的峰值时间点均不一样。进一步的试验显示生物钟基因表达的空间波动在器官内和器官间均能够传播。通过结合建模与试验的结果，作者发现这些空间波动是器官与局部的生物钟周期不一致所导致的，而不是器官与长距离信号转导之间的作用。进一步的试验显示内源性的生物钟周期不一致引起的生物钟基因表达空间波动可以由输入到生物钟的信号的器官特异性所产生。作者通过利用光照和代谢物信号，以及遗传扰动调整生物钟周期进一步验证了这一点。本文的研究结果揭示了植物的生物钟可以通过器官特异性的输入设定为局部周期，但也可以通过生物钟基因表达的空间波动协调整个植株的生物钟。

通讯：James C. W. Locke  (https://www.slcu.cam.ac.uk/people/locke-james)

个人简介：2000年，沃里克大学，学士；沃里克大学，博士 。

研究方向：利用单细胞延时显微镜、数学建模和合成生物学方法来理解动态基因调控。

doi: https://doi.org/10.1371/journal.pbio.3000407

Journal: PLOS Biology

Published date: August 15, 2019