Project #1: Function of photobodies in light signaling. (NIGMS, R01GM087388)

Photobodies are membraneless subnuclear organelles that consist of the photoreceptors phytochromes and phytochrome signaling components. At the cellular level, photobody formation is one of the earliest light responses. Increasing in light intensity initiates the biogenesis of small photobodies and promotes the assembly of small photobodies into a few large photobodies. The function of photobodies in light signaling remains elusive. We have performed a forward genetic screen to identify mutants 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 stability and activity in the regulation of light responsive genes.

– Qiu, Y., Pasoreck, E.K., Reddy, A.K., Nagatani, A., Ma, W., Chory, J., Chen, M. (2017) Mechanism of early light signaling by the carboxy-terminal output module of Arabidopsis phytochrome B. Nat Commun 8(1):1905. doi: 10.1038/s41467-017-02062-6.
– 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: Spatial genome reorganization by plant light signaling.

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 photosynthetic genes, such as the CAB1 locus, in Arabidopsis are rapidly relocated from the nuclear interior to the nuclear periphery during their transcriptional activation. The repositioning of CAB1 to the nuclear periphery is controlled by phytochromes and phytochrome signaling components. Our study of the positioning of the photosynthetic genes provides the initial evidence demonstrating the biological importance of gene positioning in plants. We currently use CAB1 as a model to investigate mechanisms of gene repositioning by cell signaling.

– 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 light signaling in controlling chloroplast biogenesis.

The biogenesis of photosynthetically active chloroplasts 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 that have been ignored by previous genetic studies, we hypothesized that additional phytochrome signaling components required for chloroplast development remain uncharacterized. 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).