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

Cell Syst. 2018 Dec 26;7(6):643-655.e9. doi: 10.1016/j.cels.2018.10.011. Epub 2018 Nov 28.

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 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.

Keywords: FLC; FLOWERING LOCUS C; VERNALIZATION INSENSITIVE3; VIN3; climate change; epigenetics; gene regulation; mathematical modeling; phenology; temperature sensing; vernalization.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics*
  • Arabidopsis / physiology
  • Arabidopsis Proteins / genetics*
  • Climate Change
  • DNA-Binding Proteins / genetics*
  • Epigenesis, Genetic*
  • Flowers / genetics
  • Flowers / physiology
  • Gene Expression Regulation, Plant*
  • Gene Regulatory Networks
  • MADS Domain Proteins / genetics*
  • Models, Biological
  • Seasons
  • Thermosensing
  • Transcription Factors / genetics*

Substances

  • Arabidopsis Proteins
  • DNA-Binding Proteins
  • At5g10140 protein, Arabidopsis
  • MADS Domain Proteins
  • Transcription Factors
  • VIN3 protein, Arabidopsis

Associated data

  • figshare/10.6084/m9.figshare.7346552