IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-34893-3.html
   My bibliography  Save this article

Structural mechanism of signal transduction in a phytochrome histidine kinase

Author

Listed:
  • Weixiao Yuan Wahlgren

    (University of Gothenburg)

  • Elin Claesson

    (University of Gothenburg)

  • Iida Tuure

    (University of Jyvaskyla)

  • Sergio Trillo-Muyo

    (University of Gothenburg)

  • Szabolcs Bódizs

    (University of Gothenburg)

  • Janne A. Ihalainen

    (University of Jyvaskyla)

  • Heikki Takala

    (University of Jyvaskyla
    University of Helsinki)

  • Sebastian Westenhoff

    (University of Gothenburg
    Uppsala University)

Abstract

Phytochrome proteins detect red/far-red light to guide the growth, motion, development and reproduction in plants, fungi, and bacteria. Bacterial phytochromes commonly function as an entrance signal in two-component sensory systems. Despite the availability of three-dimensional structures of phytochromes and other two-component proteins, the conformational changes, which lead to activation of the protein, are not understood. We reveal cryo electron microscopy structures of the complete phytochrome from Deinoccocus radiodurans in its resting and photoactivated states at 3.6 Å and 3.5 Å resolution, respectively. Upon photoactivation, the photosensory core module hardly changes its tertiary domain arrangement, but the connector helices between the photosensory and the histidine kinase modules open up like a zipper, causing asymmetry and disorder in the effector domains. The structures provide a framework for atom-scale understanding of signaling in phytochromes, visualize allosteric communication over several nanometers, and suggest that disorder in the dimeric arrangement of the effector domains is important for phosphatase activity in a two-component system. The results have implications for the development of optogenetic applications.

Suggested Citation

  • Weixiao Yuan Wahlgren & Elin Claesson & Iida Tuure & Sergio Trillo-Muyo & Szabolcs Bódizs & Janne A. Ihalainen & Heikki Takala & Sebastian Westenhoff, 2022. "Structural mechanism of signal transduction in a phytochrome histidine kinase," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34893-3
    DOI: 10.1038/s41467-022-34893-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-34893-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-34893-3?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Jeremiah R. Wagner & Joseph S. Brunzelle & Katrina T. Forest & Richard D. Vierstra, 2005. "A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome," Nature, Nature, vol. 438(7066), pages 325-331, November.
    2. Hua Li & E. Sethe Burgie & Zira T. K. Gannam & Huilin Li & Richard D. Vierstra, 2022. "Plant phytochrome B is an asymmetric dimer with unique signalling potential," Nature, Nature, vol. 604(7904), pages 127-133, April.
    3. Anselm Levskaya & Aaron A. Chevalier & Jeffrey J. Tabor & Zachary Booth Simpson & Laura A. Lavery & Matthew Levy & Eric A. Davidson & Alexander Scouras & Andrew D. Ellington & Edward M. Marcotte & Chr, 2005. "Engineering Escherichia coli to see light," Nature, Nature, vol. 438(7067), pages 441-442, November.
    4. Jon Hughes & Tilman Lamparter & Franz Mittmann & Elmar Hartmann & Wolfgang Gärtner & Annegret Wilde & Thomas Börner, 1997. "A prokaryotic phytochrome," Nature, Nature, vol. 386(6626), pages 663-663, April.
    5. Martina Legris & Yetkin Çaka Ince & Christian Fankhauser, 2019. "Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. E. Sethe Burgie & Katherine Basore & Michael J. Rau & Brock Summers & Alayna J. Mickles & Vadim Grigura & James A. J. Fitzpatrick & Richard D. Vierstra, 2024. "Signaling by a bacterial phytochrome histidine kinase involves a conformational cascade reorganizing the dimeric photoreceptor," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Stefanie S. M. Meier & Elina Multamäki & Américo T. Ranzani & Heikki Takala & Andreas Möglich, 2024. "Leveraging the histidine kinase-phosphatase duality to sculpt two-component signaling," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. E. Sethe Burgie & Katherine Basore & Michael J. Rau & Brock Summers & Alayna J. Mickles & Vadim Grigura & James A. J. Fitzpatrick & Richard D. Vierstra, 2024. "Signaling by a bacterial phytochrome histidine kinase involves a conformational cascade reorganizing the dimeric photoreceptor," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Giacomo Salvadori & Veronica Macaluso & Giulia Pellicci & Lorenzo Cupellini & Giovanni Granucci & Benedetta Mennucci, 2022. "Protein control of photochemistry and transient intermediates in phytochromes," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    3. Ruth Jean Ae Kim & De Fan & Jiangman He & Keunhwa Kim & Juan Du & Meng Chen, 2024. "Photobody formation spatially segregates two opposing phytochrome B signaling actions of PIF5 degradation and stabilization," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Zenglin Li & David J. Sheerin & Edda Roepenack-Lahaye & Mark Stahl & Andreas Hiltbrunner, 2022. "The phytochrome interacting proteins ERF55 and ERF58 repress light-induced seed germination in Arabidopsis thaliana," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    5. Yetkin Çaka Ince & Johanna Krahmer & Anne-Sophie Fiorucci & Martine Trevisan & Vinicius Costa Galvão & Leonore Wigger & Sylvain Pradervand & Laetitia Fouillen & Pierre Delft & Manon Genva & Sebastien , 2022. "A combination of plasma membrane sterol biosynthesis and autophagy is required for shade-induced hypocotyl elongation," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    6. Juan Du & Keunhwa Kim & Meng Chen, 2024. "Distinguishing individual photobodies using Oligopaints reveals thermo-sensitive and -insensitive phytochrome B condensation at distinct subnuclear locations," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    7. Zomorrodi, Ali R. & Maranas, Costas D., 2014. "Coarse-grained optimization-driven design and piecewise linear modeling of synthetic genetic circuits," European Journal of Operational Research, Elsevier, vol. 237(2), pages 665-676.
    8. Urszula Piskurewicz & Maria Sentandreu & Mayumi Iwasaki & Gaëtan Glauser & Luis Lopez-Molina, 2023. "The Arabidopsis endosperm is a temperature-sensing tissue that implements seed thermoinhibition through phyB," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    9. Yu-Yu Cheng & Zhengyi Chen & Xinyun Cao & Tyler D. Ross & Tanya G. Falbel & Briana M. Burton & Ophelia S. Venturelli, 2023. "Programming bacteria for multiplexed DNA detection," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    10. Chanhee Kim & Yongmin Kwon & Jaehoon Jeong & Minji Kang & Ga Seul Lee & Jeong Hee Moon & Hyo-Jun Lee & Youn-Il Park & Giltsu Choi, 2023. "Phytochrome B photobodies are comprised of phytochrome B and its primary and secondary interacting proteins," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    11. Derren J Heyes & Basile Khara & Michiyo Sakuma & Samantha J O Hardman & Ronan O'Cualain & Stephen E J Rigby & Nigel S Scrutton, 2012. "Ultrafast Red Light Activation of Synechocystis Phytochrome Cph1 Triggers Major Structural Change to Form the Pfr Signalling-Competent State," PLOS ONE, Public Library of Science, vol. 7(12), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34893-3. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.