Research
Research Area #1: Photobodies in light signaling.
We study how the plant photoreceptor and thermosensor phytochrome B (phyB) controls gene expression through dynamic assembly and disassembly of the phyB-containing subnuclear membraneless organelles or biomolecular condensates, named photobodies. We aim to elucidate the mechanisms of the formation, function, and regulation of photobodies in phyB signaling and the environmental control of gene expression. Accomplishments include the determination of intrinsic phyB domains as well as extrinsic factors required for photobody formation. We showed that photobody localization is mediated by phyB’s C-terminal signal-output module, specifically by the dimerization/oligomerization of the histidine-kinase-like domain. Using forward genetic screens, we identified three novel phyB signaling components required for photobody formation, including HEMERA, RCB, and NCP. Our molecular genetic studies link photobodies to the regulation of the stability and activity of a group of nodal transcriptional regulators called Phytochrome-Interacting Factors (PIFs). These breakthroughs opened a new avenue to elucidate the mechanism of light and temperature signaling in plants and established photobody as a genetic experimental model to understand the general principles of subnuclear biomolecular condensates in cell signaling and transcriptional regulation.
– Kim, RJ, Fan, D, He, J, Kim, K, Du J, Chen M (2023) Photobody formation spatially segregates two opposing phytochrome B actions to titrate plant environmental responses. bioRxiv doi: https://doi.org/10.1101/2023.11.12.566724.
– Liu, W, Lowrey, H, Leung, CC, Adamchek, C, Du, J, He, J, Chen, M, Gendron JM (2023) The circadian clock regulates PIF3 protein stability in parallel to red light. bioRxiv doi: https://doi.org/10.1101/2023.09.18.558326.
– Yoo, C.Y., He, J., Sang, Q., Qiu, Y., Long, L., Kim, R.J., Chong, E., Hahm, J., Morffy, N., Zhou, P., Strader, L.C., Nagatani, A., Mo, B., Chen, X., Chen, M. (2021) Direct photoresponsive inhibition of a p53-like transcriptional activation domain in PIF3 by Arabidopsis phytochrome B. Nat Commun 12:5614.
– Hahm, J., Kim, K., Qiu, Y., Chen, M. (2020) Increasing ambient temperature progressively disassembles Arabidopsis phytochrome B from individual photobodies with distinct thermostabilities. Nat Commun 11:1660.
– Yoo, C.Y., Pasoreck, E.K., Wang, H., Cao, J., Blaha, G.M., Weigel, D., Chen, M. (2019) Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling. Nat Commun 10:2629. doi: 10.1038/s41467-019-10518-0.
– Qiu, Y., Li, M., Kim, R.J., Moore, C.M., Chen, M. (2019) Daytime temperature is sensed by phytochrome B in Arabidopsis through a transcriptional activator HEMERA. Nat Commun 10:140. doi: 10.1038/s41467-018-08059-z.
– 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.
– 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).
– Chen, M., Chory, J., Fankhauser, C. (2004). Light signal transduction in higher plants. Annu Rev Genet 38:87-117.
Research Area #2: Daytime high-temperature signaling.
Increases in global temperature are expected to drastically reduce crop productivity, understanding the mechanism of temperature signaling has become imminent to create a knowledge base for devising strategies to sustain crop production on a warming planet. Warm temperatures usually coincide with high light conditions during the daytime. In Arabidopsis, a shift in ambient growth temperature of only a few degrees can significantly alter the expression of hundreds of temperature-responsive genes, resulting in dramatic adaptive responses in plant development, growth, metabolism, and immunity; these responses are collectively referred to as thermomorphogenesis. We showed that phytochrome B (phyB) mediates daytime temperature sensing in Arabidopsis via temperature-responsive photobody dynamics as well as HMR- and RCB-dependent stabilization of the central thermal regulator PIF4. We currently focus on elucidating the mechanism of early temperature signaling in the control of temperature-responsive genes.
– Quint M, Delker C, Balasubramanian S, Balcerowicz M, Casal JJ, Castroverde CDM, Chen M, Chen X, De Smet I, Fankhauser C, Franklin KA, Halliday KJ, Hayes S, Jiang D, Jung JH, Kaiserli E, Kumar SV, Maag D, Oh E, Park CM, Penfield S, Perrella G, Prat S, Reis RS, Wigge PA, Willige BC, van Zanten M. (2023) 25 years of thermomorphogenesis research: milestones and perspectives. Trends Plant Sci. doi: 10.1016/j.tplants.2023.07.001.
– Sang Q, Fan L, Liu T, Qiu Y, Du J, Mo B, Chen M*, Chen X*. (2023) MicroRNA156 conditions auxin sensitivity to enable growth plasticity in response to environmental changes in Arabidopsis. Nat Commun 14:1449.
– Qiu, Y.*, Pasoreck, E.K., Yoo, C.Y., He, J., Wang, H., Li, M., Larsen, H.D., Cheung, S., Chen, M.* (2021) RCB initiates Arabidopsis thermomorphogenesis by stabilizing the thermoregulator PIF4 in the daytime. Nat Commun 12:2042.
– Hahm, J., Kim, K., Qiu, Y., Chen, M. (2020) Increasing ambient temperature progressively disassembles Arabidopsis phytochrome B from individual photobodies with distinct thermostabilities. Nat Commun 11:1660.
– Qiu, Y., Li, M., Kim, R.J., Moore, C.M., Chen, M. (2019) Daytime temperature is sensed by phytochrome B in Arabidopsis through a transcriptional activator HEMERA. Nat Commun 10:140. doi: 10.1038/s41467-018-08059-z.
Research Area #3: Anterograde signaling for controlling chloroplast biogenesis.
Our molecular genetic studies of phytochrome signaling serendipitously uncovered a nucleus-to-plastid or anterograde signaling pathway linking phytochrome signaling in the nucleus to the regulation of plastid gene expression during chloroplast biogenesis. We showed that phytochrome-mediated degradation of nuclear repressors of chloroplast biogenesis, particularly the PIFs, triggers light-dependent assembly and activation of the bacterial-type plastidic RNA polymerase for the transcription of plastid-encoded photosynthesis genes. We revealed that the nucleus-to-plastid signaling pathway is unexpectedly mediated by dual-targeted signaling components, including HMR, RCB, and NCP. These breakthroughs opened the way to understand how light signaling controls chloroplast biogenesis in plants and how nuclear and organellar gene expression are coordinated by cell signaling.
– Hwang Y., Han S, Yoo C.Y., Hong L., You C., Le B.H., Shi H., Zhong S., Hoecker U., Chen X., Chen M. (2022) Anterograde signaling controls plastid transcription via sigma factors separately from nuclear photosynthesis genes. Nat Commun 13:7440.
– Yoo, C.Y., He, J., Sang, Q., Qiu, Y., Long, L., Kim, R.J., Chong, E., Hahm, J., Morffy, N., Zhou, P., Strader, L.C., Nagatani, A., Mo, B., Chen, X., Chen, M. (2021) Direct photoresponsive inhibition of a p53-like transcriptional activation domain in PIF3 by Arabidopsis phytochrome B. Nat Commun 12:5614.
– Qiu, Y.*, Pasoreck, E.K., Yoo, C.Y., He, J., Wang, H., Li, M., Larsen, H.D., Cheung, S., Chen, M.* (2021) RCB initiates Arabidopsis thermomorphogenesis by stabilizing the thermoregulator PIF4 in the daytime. Nat Commun 12:2042.
– Yoo CY, Han S, Chen M. (2020) Nucleus-to-plastid phytochrome signalling in controlling chloroplast biogenesis. Annu Plant Rev 3:251-280. doi: 10.1002/9781119312994.apr0615.
– Yang, E.M., Yoo, C.Y., Liu, J., Wang, H., Cao, J., Li, F-W, Pryer, K.M., Sun, T., Weigel, D., Zhou, P.*, Chen, M.* (2019) NCP activates chloroplast transcription by controlling phytochrome-dependent dual nuclear and plastidial switches. Nat Commun 10:2630. doi: 10.1038/s41467-019-10517-1.
– Yoo, C.Y., Pasoreck, E.K., Wang, H., Cao, J., Blaha, G.M., Weigel, D., Chen, M. (2019) Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling. Nat Commun 10:2629. doi: 10.1038/s41467-019-10518-0.
– 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.
– Qiu, Y.*, Li, M.*, Pasoreck, E.K., Long, L., Shi, Y., Galvão, R.M., Chou, C.L., Wang, H., Sun, A.Y., Zhang, Y.C., Jiang, A., Chen, M. (2015) HEMERA couples the proteolysis and transcriptional activity of Phytochrome-Interacting Factors in Arabidopsis photomorphogenesis. Plant Cell 27:1409-1427.
Research Area #4: Spatial positioning of individual genes in plants.
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.