How plants sense temperature is a longstanding and little-understood question. Researchers have discovered some of the mechanisms involved. A recent study in Nature adds a new mechanism—among the first in which the biophysical behavior of a single protein regulates the temperature response of the entire plant, says coauthor Philip Wigge, a plant biologist at the Leibniz Institute of Vegetable and Ornamental Crops in Germany. Working in Arabidopsis, the authors of the study used genetic experiments and fluorescent imaging to reveal that the protein, ELF3, is active and represses flowering genes at low temperatures, while remaining inactive at higher temperatures that allow for gene expression.
“What is really new is they propose a mechanism, a molecular process, that’s underlying thermal responses,” says biochemist Simon Alberti at Technical University Dresden, in Germany. Alberti, who was not involved in the recent work, says that most researchers expected plants to sense temperature through some kind of signaling pathway, perhaps involving a cascade of phosphorylated molecules. “But that’s not what’s happening,” he says. “Here the protein itself detects temperature.”
Indeed, the recent study found that a specific behavior of the ELF3 protein, called phase change, controls the plant’s temperature response. Essentially, the protein is soluble and active at low temperatures, and then changes phase into an inactive and liquid droplet form at high temperatures. Wigge observed this by tagging ELF3 with green fluorescent protein in the nucleus of Arabidopsis seedlings. At low temperatures, the ELF3 was surrounded by a shell of water molecules, allowing it to float and spread evenly throughout the nucleus. At higher temperatures, however, the protein changed phase by forming liquid droplets that sequester the ELF3 protein in an inactive state. The droplets appeared as large, glowing green speckles in the nuclei of the same seedlings.
When Wigge began the recent work, he suspected ELF3 was a temperature-sensitive protein, because it’s known to be involved in a group of proteins called the Evening Complex, that suppress growth and flowering at dusk. Screening a variety of genes for varying expression with temperature confirmed his suspicions. But when Wigge examined the sequence of amino acids in the protein itself, he was surprised to find a prion-like region, which are particularly prone to phase changes. Had nature harnessed phase change and used it in a biological context to control the plant’s temperature response?
He needed to compare ELF3 with and without the prion-like region, and suspected that plants from hot climates might have lost the prion-like stretch of ELF3. Sure enough, a tropical grass lacks the prion-like region. The researchers isolated the grass’ ELF3 gene and put it into transgenic Arabidopsis, then grew about 20 of the transgenic plants at different temperatures and compared their behavior to wild type Arabidopsis under the same conditions. All the plants looked the same at low temperatures, suggesting both versions of ELF3 were functional. But at high temperatures, plants expressing Arabidopsis ELF3 accelerated their flowering, indicating the protein had phase changed and become inactive. Transgenic plants expressing grass ELF3 did not accelerate flowering, suggesting their ELF3 proteins were active and suppressing flowering. The findings strongly suggest that the prion-like region of ELF3 is the specific amino acid sequence controlling the plant’s temperature response, Wigge notes.
While this discovery confirms that ELF3 is involved in the temperature response, it may not be the major thermosensor for plants in general, cautions molecular geneticist Caroline Dean, at the John Innes Center in Norwich, United Kingdom. The field has been “somewhat obsessed” with discovering one master temperature sensing mechanism, she says, when in fact there are many thermosensory steps distributed through multiple networks. Dean and biologist Yusheng Zhao recently coauthored a July Nature paper, that also found a protein involved in the plant temperature response. However, their study spanned weeks-long rather than short-term timescales, allowing the researchers to study seasonal rather than immediate temperature perception and response. Whether ELF3 plays a large role on those longer timescales has yet to be determined.
Zhao and Dean found that the protein NTL8 is continuously produced in plant meristems, even as growth and division slow in response to winter cold. As the concentration of NTL8 rises in the cell, the protein slowly upregulates transcription of a gene known to induce flowering the following spring. Temperature-dependent rates of cell division, and the associated concentration of different proteins, could be a generic mechanism to regulate many genes in many organisms, says coauthor Zhao.
Future studies could expand this work into more plant species, Wigge notes. Climate change is driving range shifts of many species and spurring reduced yields in crops, he says, some of which might be avoided by fine-tuning the plant temperature response. The question now is how to artificially accelerate adaptation. Elucidating the suite of relevant molecular players will be key. “We really need to know the temperature perception mechanisms in the plant,” he says, “if we’re to do this in a directed way.”