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PMID: 30948632 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

PCH1 regulates light, temperature, and circadian signaling as a structural component of phytochrome B-photobodies in Arabidopsis.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 116 ·No. 17 ·2019-00-23 ·Pages 8603-8608

Huang H, McLoughlin KE, Sorkin ML, Burgie ES, Bindbeutel RK, Vierstra RD, Nusinow DA

Abstract

The members of the phytochrome (phy) family of bilin-containing photoreceptors are major regulators of plant photomorphogenesis through their unique ability to photointerconvert between a biologically inactive red light-absorbing Pr state and an active far-red light-absorbing Pfr state. While the initial steps in Pfr signaling are unclear, an early event for the phyB isoform after photoconversion is its redistribution from the cytoplasm into subnuclear foci known as photobodies (PBs), which dissipate after Pfr reverts back to Pr by far-red irradiation or by temperature-dependent nonphotochemical reversion. Here we present evidence that PHOTOPERIODIC CONTROL OF HYPOCOTYL 1 (PCH1) functions both as an essential structural component of phyB-containing PBs and as a direct regulator of thermal reversion that is sufficient to stabilize phyB as Pfr in vitro. By examining the genetic interaction between a constitutively active phyBY276H-YFP allele (YHB-YFP) and PCH1, we show that the loss of PCH1 prevents YHB from coalescing into PBs without affecting its nuclear localization, whereas overexpression of PCH1 dramatically increases PB levels. Loss of PCH1, presumably by impacting phyB-PB assembly, compromises a number of events elicited in YHB-YFP plants, including their constitutive photomorphogenic phenotype, red light-regulated thermomorphogenesis, and input of phyB into the circadian clock. Conversely, elevated levels of both phyB and PCH1 generate stable, yet far-red light-reversible PBs that persisted for days. Collectively, our data demonstrate that the assembly of PCH1-containing PBs is critical for phyB signaling to multiple outputs and suggest that altering PB dynamics could be exploited to modulate plant responses to light and temperature.

Keywords
circadian clock photobodies photomorphogenesis phytochrome thermomorphogenesis
MeSH Terms
Arabidopsis/physiology Arabidopsis Proteins/genetics,metabolism,physiology Circadian Clocks/physiology F-Box Proteins/genetics,metabolism,physiology Phytochrome B/metabolism Signal Transduction/physiology Transcription Factors/genetics,metabolism,physiology
Chemicals
Arabidopsis Proteins F-Box Proteins PHOTOPERIODIC CONTROL OF HYPOCOTYL 1 protein, Arabidopsis Transcription Factors Phytochrome B
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Huang He ORCID
Donald Danforth Plant Science Center, St. Louis, MO 63132.
McLoughlin Katrice E ORCID
Department of Biology, Washington University in St. Louis, St. Louis, MO 63130.
Sorkin Maria L ORCID
Donald Danforth Plant Science Center, St. Louis, MO 63132. | Division of Biology and Biomedical Sciences, Washington University in St. Louis, St. Louis, MO 63130.
Burgie E Sethe ORCID
Department of Biology, Washington University in St. Louis, St. Louis, MO 63130.
Bindbeutel Rebecca K ORCID
Donald Danforth Plant Science Center, St. Louis, MO 63132.
Vierstra Richard D ORCID
Department of Biology, Washington University in St. Louis, St. Louis, MO 63130.
Nusinow Dmitri A ORCID
Donald Danforth Plant Science Center, St. Louis, MO 63132; meter@danforthcenter.org.
Conflict of Interest

The authors declare no conflict of interest.

References (37)
37 references, click to expand
  1. Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis.
    J Cell Biol. 1999 May 3;145(3):437-45 PMID: 10225946
  2. Light-induced nuclear translocation of endogenous pea phytochrome A visualized by immunocytochemical procedures.
    Plant Cell. 2000 Jul;12(7):1063-78 PMID: 10899974
  3. Nucleocytoplasmic partitioning of the plant photoreceptors phytochrome A, B, C, D, and E is regulated differentially by light and exhibits a diurnal rhythm.
    Plant Cell. 2002 Jul;14(7):1541-55 PMID: 12119373
  4. Characterization of the requirements for localization of phytochrome B to nuclear bodies.
    Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):14493-8 PMID: 14612575
  5. Phytochrome structure and signaling mechanisms.
    Annu Rev Plant Biol. 2006;57:837-58 PMID: 16669784
  6. Light-independent phytochrome signaling mediated by dominant GAF domain tyrosine mutants of Arabidopsis phytochromes in transgenic plants.
    Plant Cell. 2007 Jul;19(7):2124-39 PMID: 17660358
  7. Decoding of light signals by plant phytochromes and their interacting proteins.
    Annu Rev Plant Biol. 2008;59:281-311 PMID: 18257712
  8. Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness.
    Curr Biol. 2008 Dec 9;18(23):1815-23 PMID: 19062289
  9. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4.
    Curr Biol. 2009 Mar 10;19(5):408-13 PMID: 19249207
  10. A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock.
    Science. 2009 Mar 13;323(5920):1481-5 PMID: 19286557
  11. A light-independent allele of phytochrome B faithfully recapitulates photomorphogenic transcriptional networks.
    Mol Plant. 2009 Jan;2(1):166-82 PMID: 19529817
  12. Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes.
    Cell. 2010 Jun 25;141(7):1230-40 PMID: 20603003
  13. The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth.
    Nature. 2011 Jul 13;475(7356):398-402 PMID: 21753751
  14. The Cryptochrome Blue Light Receptors.
    Arabidopsis Book. 2010 Sep 23;8:e0135 PMID: 21841916
  15. Phytochrome signaling mechanisms.
    Arabidopsis Book. 2011;9:e0148 PMID: 22303272
  16. Photoactivated phytochromes interact with HEMERA and promote its accumulation to establish photomorphogenesis in Arabidopsis.
    Genes Dev. 2012 Aug 15;26(16):1851-63 PMID: 22895253
  17. A circadian clock- and PIF4-mediated double coincidence mechanism is implicated in the thermosensitive photoperiodic control of plant architectures in Arabidopsis thaliana.
    Plant Cell Physiol. 2012 Nov;53(11):1965-73 PMID: 23037004
  18. Light-regulated gene repositioning in Arabidopsis.
    Nat Commun. 2014;5:3027 PMID: 24390011
  19. The UV-B photoreceptor UVR8: from structure to physiology.
    Plant Cell. 2014 Jan;26(1):21-37 PMID: 24481075
  20. Photobody Localization of Phytochrome B Is Tightly Correlated with Prolonged and Light-Dependent Inhibition of Hypocotyl Elongation in the Dark.
    Plant Physiol. 2014 Apr 25;165(2):595-607 PMID: 24769533
  21. Phytochrome B Nuclear Bodies Respond to the Low Red to Far-Red Ratio and to the Reduced Irradiance of Canopy Shade in Arabidopsis.
    Plant Physiol. 2014 Jun 19;165(4):1698-1708 PMID: 24948827
  22. Phytochromes: an atomic perspective on photoactivation and signaling.
    Plant Cell. 2014 Dec;26(12):4568-83 PMID: 25480369
  23. Red Light-Regulated Reversible Nuclear Localization of Proteins in Mammalian Cells and Zebrafish.
    ACS Synth Biol. 2015 Sep 18;4(9):951-8 PMID: 25803699
  24. Molecular mechanisms for mediating light-dependent nucleo/cytoplasmic partitioning of phytochrome photoreceptors.
    New Phytol. 2015 May;206(3):965-71 PMID: 26042244
  25. A Constitutively Active Allele of Phytochrome B Maintains Circadian Robustness in the Absence of Light.
    Plant Physiol. 2015 Sep;169(1):814-25 PMID: 26157113
  26. PCH1 integrates circadian and light-signaling pathways to control photoperiod-responsive growth in Arabidopsis.
    Elife. 2016 Feb 03;5:e13292 PMID: 26839287
  27. Phytochromes function as thermosensors in Arabidopsis.
    Science. 2016 Nov 18;354(6314):886-889 PMID: 27789797
  28. Phytochrome B integrates light and temperature signals in Arabidopsis.
    Science. 2016 Nov 18;354(6314):897-900 PMID: 27789798
  29. Biomolecular condensates: organizers of cellular biochemistry.
    Nat Rev Mol Cell Biol. 2017 May;18(5):285-298 PMID: 28225081
  30. The plant perceptron connects environment to development.
    Nature. 2017 Mar 15;543(7645):337-345 PMID: 28300110
  31. Photosensing and Thermosensing by Phytochrome B Require Both Proximal and Distal Allosteric Features within the Dimeric Photoreceptor.
    Sci Rep. 2017 Oct 20;7(1):13648 PMID: 29057954
  32. PCH1 and PCHL promote photomorphogenesis in plants by controlling phytochrome B dark reversion.
    Nat Commun. 2017 Dec 20;8(1):2221 PMID: 29263319
  33. The Arabidopsis phyB-9 Mutant Has a Second-Site Mutation in the VENOSA4 Gene That Alters Chloroplast Size, Photosynthetic Traits, and Leaf Growth.
    Plant Physiol. 2018 Sep;178(1):3-6 PMID: 30194261
  34. The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequences and expression of PHYD and PHYE.
    Plant Mol Biol. 1994 Jun;25(3):413-27 PMID: 8049367
  35. Quantitative analysis of Drosophila period gene transcription in living animals.
    J Biol Rhythms. 1997 Jun;12(3):204-17 PMID: 9181432
  36. Biochemical characterization of Arabidopsis wild-type and mutant phytochrome B holoproteins.
    Plant Cell. 1997 Dec;9(12):2271-80 PMID: 9437866
  37. Suppressors of an Arabidopsis thaliana phyB mutation identify genes that control light signaling and hypocotyl elongation.
    Genetics. 1998 Mar;148(3):1295-310 PMID: 9539443
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2019-00-23
Epub
2019-00-04
Pages
8603-8608
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC6486730
Subset
IM
Grants
NIGMS NIH HHS · R01 GM127892 · United States
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