PCH1 integrates circadian and light-signaling pathways to control photoperiod-responsive growth in Arabidopsis

eLife, Feb 2016

Plants react to seasonal change in day length through altering physiology and development. Factors that function to harmonize growth with photoperiod are poorly understood. Here we characterize a new protein that associates with both circadian clock and photoreceptor components, named PHOTOPERIODIC CONTROL OF HYPOCOTYL1 (PCH1). pch1 seedlings have overly elongated hypocotyls specifically under short days while constitutive expression of PCH1 shortens hypocotyls independent of day length. PCH1 peaks at dusk, binds phytochrome B (phyB) in a red light-dependent manner, and co-localizes with phyB into photobodies. PCH1 is necessary and sufficient to promote the biogenesis of large photobodies to maintain an active phyB pool after light exposure, potentiating red-light signaling and prolonging memory of prior illumination. Manipulating PCH1 alters PHYTOCHROME INTERACTING FACTOR 4 levels and regulates light-responsive gene expression. Thus, PCH1 is a new factor that regulates photoperiod-responsive growth by integrating the clock with light perception pathways through modulating daily phyB-signaling.

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PCH1 integrates circadian and light-signaling pathways to control photoperiod-responsive growth in Arabidopsis

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PCH1 integrates circadian and light- signaling pathways to control photoperiod-responsive growth in Arabidopsis He Huang 3 4 5 Chan Yul Yoo 2 3 5 Rebecca Bindbeutel 3 4 5 Jessica Goldsworthy 0 3 5 Allison Tielking 3 5 6 Sophie Alvarez 1 3 4 5 Michael J Naldrett 1 3 4 5 Bradley S Evans 3 4 5 Meng Chen 2 3 5 Dmitri A Nusinow 3 4 5 0 Michigan State University , East Lansing , United States 1 Proteomics and Metabolomics Facility, Center for Biotechnology, University of Nebraska-Lincoln , Lincoln , United States 2 Department of Botany and Plant Sciences, Institute of Integrative Genome Biology, University of California at Riverside , Riverside , United States 3 Reviewing editor: Christian S Hardtke, University of Lausanne , Switzerland 4 Donald Danforth Plant Science Center , St. Louis , United States 5 Present address: 6 Mary Institute and Saint Louis Country Day School , St. Louis , United States Plants react to seasonal change in day length through altering physiology and development. Factors that function to harmonize growth with photoperiod are poorly understood. Here we characterize a new protein that associates with both circadian clock and photoreceptor components, named PHOTOPERIODIC CONTROL OF HYPOCOTYL1 (PCH1). pch1 seedlings have overly elongated hypocotyls specifically under short days while constitutive expression of PCH1 shortens hypocotyls independent of day length. PCH1 peaks at dusk, binds phytochrome B (phyB) in a red light-dependent manner, and co-localizes with phyB into photobodies. PCH1 is necessary and sufficient to promote the biogenesis of large photobodies to maintain an active phyB pool after light exposure, potentiating red-light signaling and prolonging memory of prior illumination. Manipulating PCH1 alters PHYTOCHROME INTERACTING FACTOR 4 levels and regulates lightresponsive gene expression. Thus, PCH1 is a new factor that regulates photoperiod-responsive growth by integrating the clock with light perception pathways through modulating daily phyBsignaling. DOI: 10.7554/eLife.13292.001 Competing interests: The authors declare that no competing interests exist. Funding: See page 22 Received: 24 November 2015 Accepted: 13 January 2016 Published: 03 February 2016 Copyright Huang et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Introduction Plants have evolved to coordinate physiology and phenology with seasonal variation in the environment (Wilczek et al., 2010). These adaptations to changing day length are called photoperiodic responses, which are regulated by both the circadian clock and specific signaling pathways, including light sensory systems (Shim and Imaizumi, 2015). In plants, photoperiod regulates myriad processes, including the transition to flowering (Valverde et al., 2004), cold acclimation (Lee and Thomashow, 2012), and growth (Niwa et al., 2009; Nomoto et al., 2012). In Arabidopsis, daily hypocotyl elongation is accelerated in short days compared to long day conditions, and requires both the circadian clock and light signals to properly react to changing photoperiods (Niwa et al., 2009; Nozue et al., 2007). Circadian clocks provide an adaptive advantage by synchronizing internal physiology to the external environment, allowing for an efficient allocation of resources in plants (Dodd et al., 2005). More than 20 clock components have been characterized in Arabidopsis, forming a complex network of interlocking transcription-translation feedback loops (Hsu and Harmer, 2014; Nagel and Kay, eLife digest Most living things possess an internal “circadian” clock that synchronizes many behaviors, such as eating, resting or growing, with the day-night cycle. With the help of proteins that can detect light, known as photoreceptors, the clock also coordinates these behaviors as the number of daylight hours changes during the year. However, it is not known how the clock and photoreceptors are able to work together. The circadian clocks of animals and plants have evolved separately and use different proteins. In plants, a photoreceptor called phytochrome B responds to red light and regulates the ability of plants to grow. Most plants harness sunlight during the day, but grow fastest in the dark just before dawn. In 2015, researchers identified a new protein in a plant called Arabidopsis that is associated with several plant clock proteins and photoreceptors, including phytochrome B. However, the role of this new protein was not clear. Now, Huang et al. – including many of the researchers from the 2015 work – studied the new protein, named PCH1, in more detail. The experiments show that PCH1 is a critical link that regulates the daily growth of Arabidopsis plants in response to the number of daylight hours. PCH1 stabilizes the structure of phytochrome B so that it remains active, even in the dark. This prolonged activi (...truncated)


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He Huang, Chan Yul Yoo, Rebecca Bindbeutel, Jessica Goldsworthy, Allison Tielking, Sophie Alvarez, Michael J Naldrett, Bradley S Evans, Meng Chen, Dmitri A Nusinow. PCH1 integrates circadian and light-signaling pathways to control photoperiod-responsive growth in Arabidopsis, eLife, 2016, DOI: 10.7554/eLife.13292