Neighbour signals perceived by phytochrome B increase thermotolerance in Arabidopsis.

Due to the preeminence of reductionist approaches, understanding of plant responses to combined stresses is limited. We speculated that light-quality signals of neighbouring vegetation might increase susceptibility to heat shocks because shade reduces tissue temperature and hence the likeness of heat shocks. In contrast, plants of Arabidopsis thaliana grown under low-red/far-red ratios typical of shade were less damaged by heat stress than plants grown under simulated sunlight. Neighbour signals reduce the activity of phytochrome B (phyB), increasing the abundance of PHYTOCHROME-INTERACTING FACTORS (PIFs). The phyB mutant showed high tolerance to heat stress even under simulated sunlight, and a pif multiple mutant showed low tolerance under simulated shade. phyB and red/far-red ratio had no effects on seedlings acclimated with nonstressful warm temperatures before the heat shock. The phyB mutant showed reduced expression of several fatty acid desaturase (FAD) genes and less proportion of fully unsaturated fatty acids and electrolyte leakage of membranes exposed to heat shocks. Red-light-activated phyB also reduced thermotolerance of dark-grown seedlings but not via changes in FADs expression and membrane stability. We propose that the reduced photosynthetic capacity linked to thermotolerant membranes would be less costly under shade, where the light input limits photosynthesis.

Light Primes the Thermally Induced Detoxification of Reactive Oxygen Species During Development of Thermotolerance in Arabidopsis.

Reactive oxygen species (ROS) serve as critical signaling mediators in plant adaptation responses to environmental stimuli. ROS biosynthesis and metabolism should be tightly regulated, because they often impose oxidative damage on biological molecules, such as DNA and proteins, and on cellular structures. It is known that at high temperatures, ROS rapidly accumulate in plant tissues. Thus, a quick activation of ROS-scavenging systems is necessary for thermal adaptation. However, it is largely unknown how the thermo-induced ROS-detoxifying capacity is enhanced by environmental factors at the molecular level. Here, we demonstrated that environmental light primes the thermally induced ROS detoxification process for development of thermotolerance in Arabidopsis. While the ROS detoxification capacity was markedly enhanced in light-pre-treated plants at high temperatures, its enhancement was not as evident in dark-pre-treated plants. ASCORBATE PEROXIDASE 2 (APX2) is a representative ROS-scavenging enzyme that is activated under heat stress conditions. It was observed that the thermal induction of the APX2 gene was more prominent in light-pre-treated plants than in dark-pre-treated plants. Notably, the light-gated APX2 gene induction was compromised in Arabidopsis mutants lacking the red light photoreceptor phytochrome B (phyB). Furthermore, exogenous application of the antioxidant ascorbate recovered the heat-sensitive phenotype of the phyB mutant. These observations indicate that light-primed ROS-detoxifying capability is intimately linked with the induction of thermotolerance. We propose that the phyB-mediated light priming of ROS detoxification is a key component of thermotolerant adaptation in plants.

Light priming of thermotolerance development in plants.

It is widely perceived that plant responses to environmental temperatures are profoundly influenced by light conditions. However, it is unknown how light signals modulate plant thermal responses and what photoreceptors are responsible for the light regulation of thermal adaptive process. We have recently reported that phytochrome B (phyB)-mediated red light signals prime the ASCORBATE PEROXIDASE 2 (APX2)-mediated detoxification reaction of reactive oxygen species (ROS), a well-known biochemical process that mediates the acquisition of thermotolerance under high temperature conditions. It is interesting that red light influences the HEAT SHOCK FACTOR A1 (HSFA1)-stimulated activation of the APX2 transcription, which is otherwise responsive primarily to stressful high temperatures. Blue light also efficiently primes the APX2-mediated induction of thermotolerance. In natural habitats, temperatures fluctuate according to the light/dark cycles with temperature peaks occurring during the daytime. It is thus apparent that plants utilize light information to prepare for upcoming high temperature spells.

A reversible light- and genotype-dependent acquired thermotolerance response protects the potato plant from damage due to excessive temperature.

MAIN CONCLUSION: A powerful acquired thermotolerance response in potato was demonstrated and characterised in detail, showing the time course required for tolerance, the reversibility of the process and requirement for light. Potato is particularly vulnerable to increased temperature, considered to be the most important uncontrollable factor affecting growth and yield of this globally significant crop. Here, we describe an acquired thermotolerance response in potato, whereby treatment at a mildly elevated temperature primes the plant for more severe heat stress. We define the time course for acquiring thermotolerance and demonstrate that light is essential for the process. In all four commercial tetraploid cultivars that were tested, acquisition of thermotolerance by priming was required for tolerance at elevated temperature. Accessions from several wild-type species and diploid genotypes did not require priming for heat tolerance under the test conditions employed, suggesting that useful variation for this trait exists. Physiological, transcriptomic and metabolomic approaches were employed to elucidate potential mechanisms that underpin the acquisition of heat tolerance. This analysis indicated a role for cell wall modification, auxin and ethylene signalling, and chromatin remodelling in acclimatory priming resulting in reduced metabolic perturbation and delayed stress responses in acclimated plants following transfer to 40 °C.

Chloroplast Signaling Gates Thermotolerance in Arabidopsis.

Temperature is a key environmental variable influencing plant growth and survival. Protection against high temperature stress in eukaryotes is coordinated by heat shock factors (HSFs), transcription factors that activate the expression of protective chaperones such as HEAT SHOCK PROTEIN 70 (HSP70); however, the pathway by which temperature is sensed and integrated with other environmental signals into adaptive responses is not well understood. Plants are exposed to considerable diurnal variation in temperature, and we have found that there is diurnal variation in thermotolerance in Arabidopsis thaliana, with maximal thermotolerance coinciding with higher HSP70 expression during the day. In a forward genetic screen, we identified a key role for the chloroplast in controlling this response, suggesting that light-induced chloroplast signaling plays a key role. Consistent with this, we are able to globally activate binding of HSFA1a to its targets by altering redox status in planta independently of a heat shock.