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Temperature Sensing Is Distributed throughout the Regulatory Network that Controls FLC Epigenetic Silencing in Vernalization

Antoniou-Kourounioti, Rea L. ; Hepworth, Jo ; Heckmann, Amélie ; Duncan, Susan ; Qüesta, Julia ; Rosa, Stefanie ; Säll, Torbjörn LU ; Holm, Svante ; Dean, Caroline and Howard, Martin (2018) In Cell systems 7(6). p.9-655
Abstract

Many organisms need to respond to complex, noisy environmental signals for developmental decision making. Here, we dissect how Arabidopsis plants integrate widely fluctuating field temperatures over month-long timescales to progressively upregulate VERNALIZATION INSENSITIVE3 (VIN3) and silence FLOWERING LOCUS C (FLC), aligning flowering with spring. We develop a mathematical model for vernalization that operates on multiple timescales—long term (month), short term (day), and current (hour)—and is constrained by experimental data. Our analysis demonstrates that temperature sensing is not localized to specific nodes within the FLC network. Instead, temperature sensing is broadly distributed, with each thermosensory process responding to... (More)

Many organisms need to respond to complex, noisy environmental signals for developmental decision making. Here, we dissect how Arabidopsis plants integrate widely fluctuating field temperatures over month-long timescales to progressively upregulate VERNALIZATION INSENSITIVE3 (VIN3) and silence FLOWERING LOCUS C (FLC), aligning flowering with spring. We develop a mathematical model for vernalization that operates on multiple timescales—long term (month), short term (day), and current (hour)—and is constrained by experimental data. Our analysis demonstrates that temperature sensing is not localized to specific nodes within the FLC network. Instead, temperature sensing is broadly distributed, with each thermosensory process responding to specific features of the plants’ history of exposure to warm and cold. The model accurately predicts FLC silencing in new field data, allowing us to forecast FLC expression in changing climates. We suggest that distributed thermosensing may be a general property of thermoresponsive regulatory networks in complex natural environments.

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author
; ; ; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
climate change, epigenetics, FLC, FLOWERING LOCUS C, gene regulation, mathematical modeling, phenology, temperature sensing, vernalization, VERNALIZATION INSENSITIVE3, VIN3
in
Cell systems
volume
7
issue
6
pages
9 - 655
publisher
Cell Press
external identifiers
  • pmid:30503646
  • scopus:85059223084
ISSN
2405-4712
DOI
10.1016/j.cels.2018.10.011
language
English
LU publication?
yes
id
0aa0b065-95d4-4456-9d9d-63e08ae9e437
date added to LUP
2019-01-11 12:53:40
date last changed
2024-08-07 07:49:36
@article{0aa0b065-95d4-4456-9d9d-63e08ae9e437,
  abstract     = {{<p>Many organisms need to respond to complex, noisy environmental signals for developmental decision making. Here, we dissect how Arabidopsis plants integrate widely fluctuating field temperatures over month-long timescales to progressively upregulate VERNALIZATION INSENSITIVE3 (VIN3) and silence FLOWERING LOCUS C (FLC), aligning flowering with spring. We develop a mathematical model for vernalization that operates on multiple timescales—long term (month), short term (day), and current (hour)—and is constrained by experimental data. Our analysis demonstrates that temperature sensing is not localized to specific nodes within the FLC network. Instead, temperature sensing is broadly distributed, with each thermosensory process responding to specific features of the plants’ history of exposure to warm and cold. The model accurately predicts FLC silencing in new field data, allowing us to forecast FLC expression in changing climates. We suggest that distributed thermosensing may be a general property of thermoresponsive regulatory networks in complex natural environments.</p>}},
  author       = {{Antoniou-Kourounioti, Rea L. and Hepworth, Jo and Heckmann, Amélie and Duncan, Susan and Qüesta, Julia and Rosa, Stefanie and Säll, Torbjörn and Holm, Svante and Dean, Caroline and Howard, Martin}},
  issn         = {{2405-4712}},
  keywords     = {{climate change; epigenetics; FLC; FLOWERING LOCUS C; gene regulation; mathematical modeling; phenology; temperature sensing; vernalization; VERNALIZATION INSENSITIVE3; VIN3}},
  language     = {{eng}},
  month        = {{12}},
  number       = {{6}},
  pages        = {{9--655}},
  publisher    = {{Cell Press}},
  series       = {{Cell systems}},
  title        = {{Temperature Sensing Is Distributed throughout the Regulatory Network that Controls FLC Epigenetic Silencing in Vernalization}},
  url          = {{http://dx.doi.org/10.1016/j.cels.2018.10.011}},
  doi          = {{10.1016/j.cels.2018.10.011}},
  volume       = {{7}},
  year         = {{2018}},
}