Cross-talk between the cellular redox state and the circadian system in Neurospora.

Yusuke Yoshida,Hideo Iigusa,Niyan Wang,Kohji Hasunuma

doi:10.1371/journal.pone.0028227

Yusuke Yoshida, Hideo Iigusa + Show 2 more

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https://doi.org/10.1371/journal.pone.0028227

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Abstract

The circadian system is composed of a number of feedback loops, and multiple feedback loops in the form of oscillators help to maintain stable rhythms. The filamentous fungus Neurospora crassa exhibits a circadian rhythm during asexual spore formation (conidiation banding) and has a major feedback loop that includes the FREQUENCY (FRQ)/WHITE COLLAR (WC) -1 and -2 oscillator (FWO). A mutation in superoxide dismutase (sod)-1, an antioxidant gene, causes a robust and stable circadian rhythm compared with that of wild-type (Wt). However, the mechanisms underlying the functions of reactive oxygen species (ROS) remain unknown. Here, we show that cellular ROS concentrations change in a circadian manner (ROS oscillation), and the amplitudes of ROS oscillation increase with each cycle and then become steady (ROS homeostasis). The ROS oscillation and homeostasis are produced by the ROS-destroying catalases (CATs) and ROS-generating NADPH oxidase (NOX). cat-1 is also induced by illumination, and it reduces ROS levels. Although ROS oscillation persists in the absence of frq, wc-1 or wc-2, its homeostasis is altered. Furthermore, genetic and biochemical evidence reveals that ROS concentration regulates the transcriptional function of WCC and a higher ROS concentration enhances conidiation banding. These findings suggest that the circadian system engages in cross-talk with the cellular redox state via ROS-regulatory factors.

Highlights

Biological processes, such as development and physiology are regulated via underlying circadian clock mechanisms that are synchronized with the daily light cycle of the Earth
The cellular reactive oxygen species (ROS) concentration in ras-1bd mutants displayed a circadian oscillation with a period length of approximately 22 hr; the amplitude of this oscillation gradually increased with each cycle and stabilized after 3 cycles (Fig. 1A, B and Fig. S3, S4, S5)
The peak corresponded to circadian time (CT) 12–18, and the trough corresponded to CT 6

Summary

Introduction

Biological processes, such as development and physiology are regulated via underlying circadian clock mechanisms that are synchronized with the daily light cycle of the Earth. The circadian rhythm (‘‘circa’’: around; ‘‘diem: day) is composed of selfsustaining oscillations with a period of approximately 24 hr [1]. The circadian clock is composed of three elements: an input pathway, an oscillator and an output pathway. The main oscillator in circadian clocks is likely a transcription-translation feedback loop (TTFL) that is present in a diverse range of organisms from bacteria to humans [2]. The input pathway resets the oscillator based on daily changes to external stimuli (entrainments), such as light and temperature; the oscillator can be entrained to periods around 24 hr. The oscillator controls circadian rhythmic behaviors (various biological activities and aspects of physiology) via the output pathway [2]. Not a single isolated loop, must be linked together to sustain a stable rhythm [4]

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