The PAS/LOV protein VIVID controls temperature compensation of circadian clock phase and development in Neurospora crassa

Abstract

Circadian clocks are cellular timekeepers that regulate aspects of temporal organization on daily and seasonal time scales. To allow accurate time measurement, the period lengths of clocks are conserved in a range of temperatures-a phenomenon known as temperature compensation. Temperature compensation of circadian clock period aids in maintaining a stable "target time" or phase of clock-controlled events. Here we show that the Neurospora protein VIVID (VVD) buffers the circadian system against temperature fluctuations. In vvd-null mutants, the circadian period of clock-controlled events such as asexual sporulation (conidiation) is temperature compensated, but the phase of this clock time marker is not. Consistent with delayed conidiation at lower temperatures in vvd KO strains, the levels of vvd gene products in the wild type increase with decreasing temperatures. Moreover, vvd C108A mutants that lack the light function of VVD maintain a dark activity that transiently influences the phase of conidiation, indicating that VVD influences the time of conidiation downstream from the clock. FREQUENCY (FRQ) phosphorylation is altered in a vvdKO strain, suggesting a mechanism by which VVD can influence the timing of clock-controlled processes in the dark. Thus, temperature compensation of clock-controlled output is a key factor in maintaining temperature compensation of the entire circadian system.[Keywords: Neurospora; circadian clock; temperature compensation; period; phase; VVD] Supplemental material is available at http://www.genesdev.org.

Rhythmic Conidiation in Constant Light inVividMutants ofNeurospora crassa

“…The vvd mutation delays the phase of the first band in DD and this effect is more prominent at lower temperatures; VVD may normally act to compensate for temperature effects on the rate of conidiation (Hunt et al 2007). Vvd mutants show an exaggerated phaseresetting response to light pulses, consistent with the function of wild-type VVD in downregulating rapid responses to light (Heintzen et al 2001).…”

“…This establishes a function for VVD as an activator of some light-induced genes, and it may be the absence of this function that allows the vvd mutant strains in our experiments to express a rhythm of conidiation in LL. Hunt et al (2007) have proposed a role for VVD in the conidiation output pathway, and this may explain the activation of continuous conidiation, rather than rhythmic conidiation, in LL in vvd 1 . The loss of VVD protein in the vvd mutants would remove this activation function of VVD and allow expression of the conidiation rhythm in LL.…”

Physical interaction between VIVID and white collar complex regulates photoadaptation inNeurospora

“…Considerable evidence suggests that VVD regulates the transcriptional activity of the WCC in mediating photoadaptation in constant light as well as several other properties associated with the circadian clock under free-running conditions (7,21,24,26). Despite the genetic relationship between VVD and the WCC, biochemical studies examining their physical interaction and subcellular localization have not shown direct interactions or colocalization.…”

“…Loss-of-function vvd mutants were originally identified by the unique appearance of the bright orange conidia while grown in constant light (23), presumably attributable to the persistent activation of carotenoid biosynthesis (7). In addition to its function in attenuating the direct light response in Neurospora, VVD has been shown to take part in regulating various circadian clock properties, most likely through its effects on the WCC, including gating of light input to the clock (21), maintenance of the clock during the light phase (24,25), and temperature compensation of the circadian phase (26). Despite accumulating genetic and molecular evidence supporting the connection between VVD and WCC, no mechanistic explanation for the relationship has been proposed.…”

Synchronization of theDrosophilaCircadian Clock by Temperature Cycles

“…Although several interesting models have been developed, and clock genes have been shown "to be important" for temperaturecompensation, the mechanisms are not understood on a molecular level (Huang et al 1995;Leloup and Goldbeter 1997;Sawyer et al 1997;Ruoff et al 2005;Hunt et The natural light/dark and temperature cycles are considered to be the most prominent factors that synchronize circadian clocks with the environment. Understanding the principles of temperature entrainment significantly lags behind our current knowledge of light entrainment in any organism subject to circadian research.…”