Ph.D. University of Sydney, Australia, 1968
B.S. Agriculture University of Sydney, Australia, 1964
We research molecular mechanisms by which light regulates gene expression in plants, focusing on the phytochrome (phy) family of sensory photoreceptors. The photoreceptor molecule acts as a biological switch that upon perception of the light signal, triggers changes in transcription detectable within 5 minutes of the stimulus. We have also developed a novel light-switchable gene promoter system potentially usable in any light-accessible eukaryotic cell system for rapid, conditional induction or repression of expression.
Molecular genetics of phytochrome action
We are interested in understanding the molecular mechanism by which light regulates gene expression in plants. Our research program is focused on the phytochromes, the most extensively characterized family of plant sensory photoreceptors. The photoreceptor molecule functions as a biological switch that, upon perception of the light signal, triggers changes in transcription which are detectable within 5 minutes of the stimulus.
Plants monitor and respond developmentally to an array of environmental light signals.
What molecular mechanisms are involved in the perception, interpretation and transduction of those signals?
We employ the following fourfold general strategy to approach this problem:
- Examine the phytochrome molecule for clues to its photosensory function and mechanism of action using structural analysis, phytochrome-defective mutants and overexpression of mutagenized phytochromes in transgenic Arabidopsis.
- Study genes under phytochrome control to identify promoter DNA elements and transcription factors involved in induction or repression of expression.
- Identify signal transduction pathway components between the photoreceptor and the genes it regulates using forward and reverse genetic screens for signaling-defective mutants, and molecular interaction screens for phytochrome-interacting proteins.
- Dissect the primary transcriptional networks that orchestrate the expression of downstream genes responsible for elaborating light-regulated development, using RNA-seq expression profiling.
Our data show that the phytochromes signal directly to photoresponsive genes by light induced translocation from the cytoplasm into the nucleus, followed by specific physical interaction with promoter-bound transcription factors (called PIFs, for phy-interacting factors) of the basic helix-loop-helix (bHLH) class. The data also show that genes encoding a master-set of diverse transcriptional regulators, which orchestrate downstream expression in the transcriptional network, are direct targets of this signaling pathway.
We have obtained evidence that light-induced activation of the phytochrome molecule induces intranuclear phosphorylation of the bHLH transcription factor, PIF3, preceding its ubiquitination and proteosome-mediated degradation. These data suggest that phy-induced phosphorylation of target proteins may represent the primary intermolecular signaling transaction of the activated photoreceptor.
Zhang, Y., Pfeiffer, A., Tepperman, J. M., Dalton-Roesler, J., Leivar, P., Gonzalez Grandio, E., and Quail, P. H. 2020. Central clock components modulate plant shade avoidance by directly repressing transcriptional activation activity of PIF proteins. Proc Natl Acad Sci, 117: 3261–3269.
Ni, W., Xu, S. -L, González-Grandío, E., Chalkley, R. J., Huhmer, A. F. R., Burlingame, A., Wang, Z. -Y and Quail, P.H. 2017. PPKs mediate direct signal transfer from phytochrome photoreceptors to transcription factor PIF3. Nature Comm 8:15236
Soy, J., Leivar, P., González-Schain, N., Martín, G., Diaz, C., Sentandreu, M., Bassem Al Sady, B., Quail, P. H., and Monte E. 2016. Molecular convergence of clock and photosensory pathways through PIF3-TOC1 interaction and co-occupancy of target promoters. Proc Natl Acad Sci, 113: 4870-4875.
Pfeiffer, A., Shi, H., Tepperman, J. M., Zhang, Y. and Quail, P. H. 2014. Combinatorial Complexity in a Transcriptionally-centered Signaling Hub in Arabidopsis. Mol Plant 7: 1598-1618.
Ni, W., Xu, S., Tepperman, J. M., Stanley, D.J., Maltby, D.A., Gross, John, D. Burlingame, Alma L., Wang, Z., Quail1, P.H. (2014). A mutually assured destruction mechanism attenuates light signaling in Arabidopsis. Science, 344: 1160-1164.
Zhang, Y., Mayba, O., Pfeiffer, A., Shi, H., Tepperman, J.M., Speed, T.P., and Quail, P.H. (2013). A Quartet of PIF bHLH Factors Provides a Transcriptionally Centered Signaling Hub That Regulates Seedling Morphogenesis through Differential Expression-Patterning of Shared Target Genes in Arabidopsis. PLoS Genet, 9: (1) e1003244
Leivar, P., Monte, E., Cohn, M.M., and Quail, P.H. (2012). Phytochrome Signaling in Green Arabidopsis Seedlings: Impact Assessment of a Mutually Negative phyB-PIF Feedback Loop. Molecular Plant, 5: (3) 734-749
Leivar, P., Tepperman, J.M., Cohn, M.M., Monte, E., Al-Sady, B., Erickson, E., and Quail, P.H. (2012). Dynamic Antagonism between Phytochromes and PIF Family Basic Helix-Loop-Helix Factors Induces Selective Reciprocal Responses to Light and Shade in a Rapidly Responsive Transcriptional Network in Arabidopsis. The Plant Cell Online, 24: (4) 1398-1419
Soy, J., Leivar, P., Gonzalez-Schain, N., Sentandreu, M., Prat, S., Quail, P.H., and Monte, E. (2012). Phytochrome-imposed oscillations in PIF3 protein abundance regulate hypocotyl growth under diurnal light/dark conditions in Arabidopsis. The Plant Journal, 71: (3) 390-401
Leivar, P. and Quail, P. H. (2011). PIFs: Pivotal components in a cellular signaling hub. Trends in Plant Science. 16: 19-28.
Quail, P. H. 2010. Phytochromes. Current Biology, 20: R504-R507.
Franklin, K. A. and P. H. Quail (2010). Phytochrome functions in Arabidopsis development. . J. Exp. Bot., 61:11-14.
Leivar, P., J. M. Tepperman, et al. (2009). "Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings." Plant Cell 21(11): 3535-3553.
Kikis, E. A., Y. Oka, et al. (2009). Residues clustered in the light-sensing knot of phytochrome B are necessary for conformer-specific binding to signaling partner PIF3. PLoS Genet 5(1): e1000352.
Al-Sady, B., E. A. Kikis, et al. (2008). Mechanistic duality of transcription factor function in phytochrome signaling. Proc Natl Acad Sci U S A 105(6): 2232-2237.
Leivar, P., E. Monte, et al. (2008). The Arabidopsis phytochrome-interacting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels. Plant Cell 20(2): 337-352.
Leivar, P., E. Monte, et al. (2008). Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr Biol 18(23): 1815-1823.
Al-Sady B, Ni W, Kircher S, Schaefer E, Quail PH (2006). Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Molecular Cell, 23, 439-446.
Tepperman JM, Hwang YS, Quail PH.(2006) phyA Dominates in Transduction of Red-light Signals to Rapidly-responding Genes at the Initiation of Arabidopsis Seedling Deetiolation Plant J. Dec;48(5):728-42. Epub 2006 Oct 31. PMID:17076805
Monte, E.; Tepperman, J. M.; Al-Sady, B.; Kaczorowski, K. A.; Alonso, J. M.; Ecker, J. R.; Li, X.; Zhang, Y.; Quail, P. H (2004). The phytochrome-Interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development. Proc. Natl. Acad. Sci (USA), 101 : 16091-16098.
Khanna, R.; Huq, E.; Kikis, E. A.; Al-Sady, B.; Lanzatella, C.; Quail, P. H. (2004). A novel molecular recognition motif necessary for targeting photoactivated Phytochrome signalling to specific basic helix-loop-helix transcription factors. Plant Cell, 16 : 3033-304.
Huq, E.; Al-Sady, B.; Hudson, M.; Kim, C.; Apel, K.; Quail, P. H. (2004). PHYTOCHROME-INTERACTING FACTOR 1, a basic helix-loop-helix transcription factor, is a critical regulator of the chlorophyll biosynthetic pathway. Science, 305: 1937-1941.
Kaczorowski, K. A.; Quail, P. H.(2003). Arabidopsis PSEUDO-RESPONSE REGULATOR 7 (PRR7) is a signaling intermediate in phytochrome-regulated seedling deetiolation and phasing of the circadian clock. Plant Cell 15: 2654-2665
Hudson, Matthew E; Lisch, Damon R; Quail, Peter H. (2003). The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant Journal, 34:453-471.
Toledo-Ortiz, G.; Huq, E.; Quail, P. H. (2003). The Arabidopsis basic helix-loop-helix transcription factor family. Plant Cell, 15: 1749-1770.
Shimizu-Sato, S.; Huq, E.; Tepperman, J. M.; Quail, P. H. (2002). A light-switchable gene promoter system. Nature Biotechnology, 20 (10): 1041-1044.
Huq, E.; Quail, P. H. (2002).: PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO Journal, 21: 2441-2450.
Tepperman, J. M.; Zhu, T.; Chang, H. S.; Wang, X.; Quail, P. H. (2001). Multiple transcription-factor genes are early targets of phytochrome A signaling. Proc Natl Acad Sci (USA), 98 (16): 9437-9442.
The Stephen Hales Prize - American Society of Plant Biologists - 2008
Member - National Academy of Sciences - 2004
Fellow - American Association for the Advancement of Science - 2004