Review
How do plants feel the heat?

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In plants, the heat stress response (HSR) is highly conserved and involves multiple pathways, regulatory networks and cellular compartments. At least four putative sensors have recently been proposed to trigger the HSR. They include a plasma membrane channel that initiates an inward calcium flux, a histone sensor in the nucleus, and two unfolded protein sensors in the endoplasmic reticulum and the cytosol. Each of these putative sensors is thought to activate a similar set of HSR genes leading to enhanced thermotolerance, but the relationship between the different pathways and their hierarchical order is unclear. In this review, we explore the possible involvement of different thermosensors in the plant response to warming and heat stress.

Section snippets

Why is it important to study heat stress in plants?

Temperature is one of the key physical parameters affecting life on Earth. As a result, almost all living organisms have evolved signaling pathways to sense mild changes in ambient temperature and adjust their metabolism and cell function to prevent heat-related damage. Indeed, many features of the heat stress response (HSR) pathway are conserved among both prokaryotic and eukaryotic organisms 1, 2. The HSR pathway has been extensively studied in plants 3, 4, 5, 6, 7, 8, but many questions

How does heat stress affect plants?

Heat stress differentially affects the stability of various proteins, membranes, RNA species and cytoskeleton structures, and alters the efficiency of enzymatic reactions in the cell, causing a state of metabolic imbalance 22, 23, 24. Because most cellular reactions are coupled, disrupting the steady-state flux of metabolites can cause the accumulation of toxic by-products, such as reactive oxygen species (ROS). Indeed, an intimate relationship exists between oxidative stress and the HSR in

What types of heat response exist in plants?

Various treatments have been used to study heat response in plants, the most common of which is to subject plants growing under controlled conditions to an episode of severe heat stress. In Arabidopsis thaliana, for example, this entails subjecting plants growing at 21 °C to an abrupt 42–45 °C treatment for a period of 0.5–1 h. The ability of plants to respond and successfully acclimate to such treatment is generally referred to as basal thermotolerance, and is assayed by measuring plant survival

How do plants sense heat?

When an A. thaliana leaf is exposed to a rise in ambient temperature, its large surface-to-volume ratio ensures that almost all macromolecules in the cells, such as protein complexes, membranes and nucleic acid polymers, ‘perceive’ the heat simultaneously. The increased kinetic movement of these macromolecules is expected to concomitantly cause reversible physical changes, such as increased membrane fluidity, partial melting of DNA and RNA strands, protein subunit dissociation and exposure of

Sensing heat at the plasma membrane

The primary sensing event of heat stress in the moss Physcomitrella patens occurs at the plasma membrane (PM) 39, 40. A combination of electrophysiology, reporter gene assays and biochemical measurements [39] revealed that mild increases in temperature are sensed at the PM, lead to the opening of a specific calcium channel that triggers an influx of calcium into the cell, and activate the HSR. The suppression of this pathway by calcium channel blockers or chelators indicates that the calcium

Unfolded protein response (UPR) in the ER and the cytosol

The UPR is a signaling pathway activated in cells in response to stresses that impair protein stability in the endoplasmatic reticulum (ER) 15, 64. In plants, there seem to be at least two UPR pathways, one in the ER and the other in the cytosol 65, 66, 67. The UPR can be activated by heat stress, by chemicals that cause the unfolding of proteins, or by different abiotic stresses such as changes in salinity or osmotic stress [15]. The activation of the ER UPR pathway in plants involves the

Metabolic changes and ROS signaling

Because different metabolic pathways probably depend on enzymes with different sensitivities to excessive heat, it has been suggested that heat stress might uncouple some metabolic pathways and cause the accumulation of unwanted by-products, such as ROS, that could act as signals to trigger the HSR 69, 70. Nevertheless, ROS accumulation during heat stress is also an active response that is mediated by specific ROS-producing enzymes [25]. ROS accumulation can be triggered in tobacco cells by

Temperature-induced changes in histone occupancy

A screen of A. thaliana mutants impaired in heat sensing identified the gene ARP6 as involved in mediating responses to temperature change [36]. ARP6 encodes a subunit of the SWR1 complex, which is necessary for inserting the alternative histone H2A.Z into nucleosomes, instead of H2A, and could be involved in temperature sensing 73, 74, 75. Mutants lacking ARP6 have a reduced content of H2A.Z bound to their chromosomes. Interestingly, the transcriptome of arp6 null mutants grown at 12 °C is

Concluding remarks

In plants, changes in ambient temperature seem to be sensed via a complex network of molecular sensors located in different cell compartments (Figure 1, Figure 3). The sensors include a rapid PM sensing mechanism that triggers a specific inward calcium flux, UPR sensors in the ER and the cytosol, and histone decreased occupancy in the nuclei (Figure 3). The signals generated by these different sensors are probably integrated by a signal transduction network that involves calcium fluxes,

Acknowledgments

Research in the authors’ laboratories is supported by funding from the National Science Foundation (IBN-0420033, NSF-0431327, IOS-0639964 and IOS-0743954), the University of North Texas College of Arts and Sciences, the Swiss National Science Foundation (3100A0-109290), and the University of Lausanne. We thank Maude Muriset and America Farina Cuendet for technical assistance.

Glossary

Brassinosteroids
a group of plant steroid hormones that regulate growth, development and responses to different environmental stresses.
bZIP
a family of TFs that contain a basic leucine zipper (bZIP) domain and regulate many central developmental and physiological processes in plants, such as photomorphogenesis, energy homeostasis, and abiotic and biotic stress responses.
Calmodulin
a calcium-binding protein family that can bind to and regulate several different protein targets in plants.
DREB

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