Research in our lab focuses on understanding the molecular mechanisms by which plants respond to changes in their light environment. Plant development and growth are extremely plastic in response to environmental light cues. Light, perceived by photoreceptors, controls all developmental transitions in plants by reprogramming the expression of thousands of light-responsive genes in both the nuclear and plastidial genomes. However, the signaling mechanisms linking photoactivation of photoreceptors and transcriptional regulation in the nucleus and plastids are far from fully understood. We use phytochromes, the red and far-red photoreceptors, in Arabidopsis as a model to elucidate early light signaling mechanisms that control morphogenetic transitions in plant development. Our goal is also to use light signaling in Arabidopsis as a genetic model to understand evolutionarily conserved mechanisms in subnuclear organization and nuclear-organellar communication.

Project #1: Biogenesis and function of photobodies in light signaling (NIH, R01GM087388)

Photobodies are membraneless subnuclear organelles that consist of phytochromes and mediate early light signaling events. Increasing in light intensity triggers the initiation of small photobodies and promotes the assembly of small photobodies into a few large photobodies. The function of photobodies remains elusive. We developed a fluorescence-microscopy-based forward genetic screen for isolating mutants that are defective in photobody biogenesis. This screen has identified a novel phytochrome signaling component named HEMERA (HMR). Our recent studies of photobodies and HMR have provided substantial evidence linking photobodies to the proteolysis of a group of master plant growth regulators, the Phytochrome-Interacting Factors (PIFs). We currently investigate how photobodies and HMR control PIF degradation and the expression of PIF-regulated, light-responsive genes.

– Huang, H., Yoo, C., Bindbeutel, R.K., Goldsworthy, J., Tielking, A., Alvarez, S., Naldrett, M.J., Evans, B., Chen, M., Nusinow, D.A. (2016) PCH1 integrates circadian and light-signaling pathways to control photoperiod-responsive growth in Arabidopsis. eLife 5:e13292.
– Qiu, Y., Li, M., Van Buskirk, E.K., Long, L., Shi, Y., Galvão, R.M., Chou, C.L., Sun, A.Y., Zhang, Y.C., Jiang, A., Chen, M. (2015) HEMERA couples the proteolysis and activity of PHYTOCHROME INTERACTING FACTORs. Plant Cell 27(5):1409-27.
– Van Buskirk, E.K., Reddy, A.K., Nagatani, A., Chen, M. (2014) Photobody localization of phytochrome B is tightly correlated with prolonged and light-dependent inhibition of hypocotyl elongation in the dark. Plant Physiol 165(2):595-607.
– Galvão, R.M., Li, M., Kothadia, S.M., Haskel, J.D., Decker, P.V., Van Buskirk, E.K., Chen, M. (2012) Photoactivated phytochromes interact with HEMERA and promote its accumulation to establish photomorphogenesis in Arabidopsis. Genes Dev 26(16):1851-63.
– Van Buskirk E.K., Decker, P.V., Chen, M. (2012) Photobodies in light signaling. Plant Physiol 158(1):52-60.
– Chen, M.*, Chory, J.* (2011). Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol 21(11):664-71 (* Corresponding author).
– Chen, M.*, Galvão, R.M., Li, M., Burger, B., Bugea, J., Bolado, J., Chory, J.* (2010). Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 141(7): 1230-1240 (* Corresponding author).
– Fankhauser C.*, Chen, M. (2008). Transposing phytochrome into the nucleus. Trends Plant Sci 13(11):596-601 (* Corresponding author).
– Chen, M. (2008). Phytochrome nuclear body: an emerging model to study interphase nuclear dynamics and signaling. Curr Opin Plant Biol 11(5):503-8.
– Chen, M., Tao, Y., Lim, J., Shaw, A., Chory, J. (2005). Regulation of phytochrome B nuclear localization through light-dependent unmasking of nuclear localization signals. Curr Biol 15(7):637-42.
– Chen, M., Chory, J., Fankhauser, C. (2004). Light signal transduction in higher plants. Annu Rev Genet 38:87-117.
– Chen, M., Schwab, R., and Chory, J. (2003). Characterization of requirements for localization of phytochrome B to nuclear bodies. Proc Natl Acad Sci USA 100(24):14493-14498.

Project #2: Mechanisms of light-regulated gene positioning

A growing body of evidence from studies in yeast and metazoan models suggests that spatial positioning of individual genes plays an important role in transcriptional regulation. However, the mechanism controlling gene positioning is still poorly understood. We have shown that the light-inducible CAB1 locus in Arabidopsis is rapidly relocated from the nuclear interior to the nuclear periphery during its transcriptional activation. The repositioning of CAB1 to the nuclear periphery is controlled by phytochromes and some phytochrome signaling components. Moreover, CAB1 repositioning occurs as a separate regulatory step prior to full transcriptional activation. Our study of CAB1 positioning provides the first evidence demonstrating the biological importance of gene positioning in plants. We currently use CAB1 as a model to investigate mechanisms of gene repositioning in plants.

– Feng, C.-M., Qiu, Y., Van Buskirk, E.K., Yang, E.J., Chen, M. (2014) Light-regulated gene repositioning in Arabidopsis. Nat Commun 5:3027 doi: 10.1038/ncomms4027.

Project #3: Mechanism of Phytochrome signaling in controlling chloroplast biogenesis

The biogenesis of photosynthetically active chloroplast is essential for photosynthesis and autotrophic growth in plants. Although it has been well known that chloroplast development is initiated by phytochromes, the mechanism by which phytochrome signaling controls chloroplast development is still poorly understood. Recent studies of HMR, also known as pTAC12, by our lab and others unexpectedly revealed that HMR is dual-localized to the nucleus and chloroplasts. These surprising results indicate that some phytochrome signaling components play essential roles in chloroplast development. Because the hmr mutant, with both long hypocotyl and albino phenotypes, represents a novel class of light signaling mutants, which have been ignored by previous genetic studies, we hypothesized that additional phytochrome signaling components required for chloroplast development remain to be discovered. The goal of this project is to elucidate light signaling mechanisms in controlling chloroplast development.

– Nevarez P.A., Qiu, Y., Inoue, H., Yoo, C., Benfey, P.N., Schnell, D.J., Chen, M. (2017) Mechanism of dual-targeting of the phytochrome signaling component HEMERA/pTAC12 to plastids and the nucleus. Plant Physiol DOI:10.1104/pp.16.00116.
– Chen, M., Chory, J. (2011). Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol 21(11):664-71.
– Chen, M.*, Galvão, R.M., Li, M., Burger, B., Bugea, J., Bolado, J., Chory, J.* (2010). Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 141(7): 1230-1240 (* Corresponding author).