Trends in Plant Science
OpinionFeeling the Heat: Searching for Plant Thermosensors
Section snippets
What’s in a Name: A Redefinition of Thermosensors
In recent years, various plant proteins have been shown to act as thermosensors 1, 2, 3 or have been mistakenly referred to as thermosensors [4]. While the term ‘thermosensor’ or ‘thermosensory’ has been used often, most of the described molecular regulation is limited to explaining the actual response to temperature elevation [5]. But what is a true thermosensor? For all environmental responses, sensing is the primary step during which a sensor directly decodes a stimulus into cellular
Can DNA/Chromatin Structures Function as Thermosensors?
In bacteria, DNA replication and transcription is very sensitive to DNA supercoiling (see Glossary), which is highly regulated by temperature 13, 14. Further, DNA–protein structures, such as the DNA bend created by the histone-like nucleoid-structuring (H-NS) protein, can melt and allow the transcription of the virulence-regulating transcription factor virF and host invasion at the critical threshold temperature of 32°C [15].
In Arabidopsis, in response to increased temperature (above 22°C), the
RNA Thermosensors in Plants: An Unexplored Territory
RNA secondary structures regulate many RNA-related processes and such structures are sensitive to environmental changes [21]. In bacteria, some mRNA stem-loop structures can be ‘unzipped’ by high temperature, facilitating ribosome binding and translation (Figure 2B) [22]. In addition to RNA zippers, RNA can also adopt distinct stem-loop structures at different temperatures (RNA switches) that play a role in translational regulation [22]. RNA-mediated thermosensing has also been described in
What about Thermosensors for Alternative Splicing?
Alternative splicing affected by temperature has been observed frequently in plants (Figure 2C) [29]. A well-known example is the alternative splicing of pre-mRNA of FLOWERING LOCUS M (FLM), resulting in a temperature-dependent ratio of two isoforms, FLM-β and FLM-δ, where the FLM-β level mainly contributes to thermoresponsive flowering 30, 31, 32. However, the thermosensing components for this response remain unknown.
RNA secondary structures play an important role in RNA splicing regulation 29
Thermosensing via Protein Conformational Changes
Temperature may directly influence the activity of proteins. For example, the reaction rate of an enzymatic reaction increases to an optimal temperature due to the higher kinetic energy, which leads to more enzyme–substrate contacts, whereas excessively high temperature disturbs protein folding and activity [43]. In addition, proteins are dynamic structures which can be highly influenced by changes in temperature (Figure 2D) [44]. Hence, conformational changes can serve as mechanisms for direct
What about Thermosensing at the Membrane?
Besides intrinsic thermal sensitivity, in some cases, protein conformational changes are coupled to a temperature-induced change of the biochemical environment in which the protein resides. For example, membrane-associated proteins need to adapt their conformation so that their transmembrane part maintains an optimal hydrophobic contact with the lipid bilayer surrounding it (Figure 2F) [58]. Noticeably, the fluidity of the lipid bilayer is highly affected by temperature [59] and can function as
Concluding Remarks and Future Perspectives
Collectively, we would like to propose a set of criteria to which a thermosensor has to adhere (Figure 1): (1) one or several properties (such as structural features or activity) of a thermosensor need to be directly altered by temperature changes; (2) these properties are important for the functional module(s) in which the thermosensor participates and need to be efficiently and reproducibly interpreted to convey the temperature information to the response machineries; and (3) the
Acknowledgements
L.D.V is a recipient of the VIB International PhD Scholarship in Life Sciences.
Glossary
- Alternative splicing
- after transcription, in eukaryotes, the pre-mature mRNA undergoes splicing to remove introns. However, in some cases, introns will be retained in the mature mRNA or exons will be removed to finally generate different protein isoforms that may have different functions.
- DNA supercoiling
- this DNA topology can be created by over- or underwinding of the DNA double strand. Supercoiling can be lifted by topoisomerases that are specific for different types of supercoiling, a process
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