Feeling Every Bit of Winter - Distributed Temperature Sensitivity in Vernalization

Abstract

Temperature intrinsically influences all aspects of biochemical and biophysical processes. Organisms have therefore evolved strategies to buffer themselves against thermal perturbations. Many organisms also use temperature signals as cues to align behavior and development with certain seasons. These developmentally important thermosensory mechanisms have generally been studied in constant temperature conditions. However, environmental temperature is an inherently noisy signal, and it has been unclear how organisms reliably extract specific temperature cues from fluctuating temperature profiles. In this context, we discuss plant thermosensory responses, focusing on temperature sensing throughout vernalization in Arabidopsis. We highlight many different timescales of sensing, which has led to the proposal of a distributed thermosensing paradigm. Within this paradigm, we suggest a classification system for thermosensors. Finally, we focus on the longest timescale, which is most important for sensing winter, and examine the different mechanisms in which memory of cold exposure can be achieved.

Keywords: Arabidopsis; FLC; climate change; mathematical modeling; temperature fluctuations; temperature-sensing; vernalization.

Figure 1

Importance of temperature fluctuations in plant seasonal sensing. (A) Temperature profile at experimental site in Norwich, United Kingdom, measured over 200 days from September 29, 2014 (Hepworth et al., 2018). (B) Schematic of classification of days according to whether the temperature fluctuated to above 15°C or not, during the day. This classification is used in the next panel. (C) Data from Norwich Airport, United Kingdom for the indicated years. Information provided by the National Meteorological Library and Archive – Met Office, United Kingdom, under the Open Government License (The National Archives, n.d.). Schematic shows coloration for days where the temperature fluctuated above 15°C, and white for other days, as indicated in (B). The continuous white period matches winter.

Figure 2

Distributed temperature sensitivities in the regulation of FLOWERING LOCUS C (FLC) and VERNALIZATION INSENSITIVE3 (VIN3), and indirect long-term temperature sensing through NTL8 during vernalization. (A) Temperature sensitivities are widely distributed in the regulation of VIN3 and FLC during vernalization. Cold regulates VIN3 and FLC through multiple pathways: at least five separate pathways have been shown to be needed. In some cases, such as the “Long-term” pathway, the mechanism and components are known (NTL8; Zhao et al., 2020b). Known and postulated components are illustrated schematically in the diagram. (B) Temperature-dependent growth is indirectly exploited by the NTL8 protein to sense long-term cold. NTL8 concentration decreases when the plant grows fast in the warm (bottom, orange arrows/curves), but slowly increases when the plant grows slowly in the cold (top, blue arrows/curves). The slow accumulation of NTL8 protein holds the memory of cold exposure in the cold, allowing a slow increase in VIN3 concentration, which promotes the epigenetic repression of FLC – a repressor of the floral transition. Purple circles on the plant indicate NTL8 protein. The total amount of protein shown is the same in warm and cold, but the concentration is different due to the difference in growth rate.