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Heat stress adversely affects an array of molecular and cellular events in plant cells, such as denaturation of protein and lipid molecules and malformation of cellular membranes and cytoskeleton networks. Genome organization and DNA integrity are also disturbed under heat stress, and accordingly, plants have evolved sophisticated adaptive mechanisms that either protect their genomes from deleterious heat-induced damages or stimulate genome restoration responses. In particular, it is emerging that DNA damage responses are a critical defense process that underlies the acquirement of thermotolerance in plants, during which molecular players constituting the DNA repair machinery are rapidly activated. In recent years, thermotolerance genes that mediate the maintenance of genome integrity or trigger DNA repair responses have been functionally characterized in various plant species. Furthermore, accumulating evidence supports that genome integrity is safeguarded through multiple layers of thermoinduced protection routes in plant cells, including transcriptome adjustment, orchestration of RNA metabolism, protein homeostasis, and chromatin reorganization. In this review, we summarize topical progresses and research trends in understanding how plants cope with heat stress to secure genome intactness. We focus on molecular regulatory mechanisms by which plant genomes are secured against the DNA-damaging effects of heat stress and DNA damages are effectively repaired. We will also explore the practical interface between heat stress response and securing genome integrity in view of developing biotechnological ways of improving thermotolerance in crop species under global climate changes, a worldwide ecological concern in agriculture.

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Plants dynamically adapt to changing temperatures to ensure propagation and reproductive success, among which morphogenic responses to warm temperatures have been extensively studied in recent years. As readily inferred from the cyclic co-oscillations of environmental cues in nature, plant thermomorphogenesis is coordinately reshaped by various external conditions. Accumulating evidence supports that internal and developmental cues also contribute to harmonizing thermomorphogenic responses. The external and internal reshaping of thermomorphogenesis is facilitated by versatile temperature sensing and interorgan communication processes, circadian and photoperiodic gating of thermomorphogenic behaviors, and their metabolic coordination. Here, we discuss recent advances in plant thermal responses with focus on the diel and seasonal reshaping of thermomorphogenesis and briefly explore its application to developing climate-smart crops.

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Plants possess an astonishing capability of effectively adapting to a wide range of temperatures, ranging from freezing to near-boiling temperatures1,2. Yet, heat is a critical obstacle to plant survival. The deleterious effects of heat shock on cell function include misfolding of cellular proteins, disruption of cytoskeletons and membranes, and disordering of RNA metabolism and genome integrity3-5. Plants stimulate diverse heat shock response pathways in response to abrupt temperature increases. While it is known that stressful high temperatures disturb genome integrity by causing nucleotide modifications and strand breakages or impeding DNA repair6, it is largely unexplored how plants cope with heat-induced DNA damages. Here, we demonstrated that high expression of osmotically reponsive genes 1 (HOS1) induces thermotolerance by activating DNA repair components. Thermotolerance and DNA repair capacity were substantially reduced in HOS1-deficient mutants, in which thermal induction of genes encoding DNA repair systems, such as the DNA helicase RECQ2, was markedly decreased. Notably, HOS1 proteins were thermostabilized in a heat shock factor A1/heat shock protein 90 (HSP90)-dependent manner. Our data indicate that the thermoresponsive HSP90-HOS1-RECQ2 module contributes to sustaining genome integrity during the acquisition of thermotolerance, providing a distinct molecular link between DNA repair and thermotolerance.

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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.

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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.

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The circadian clock control of CONSTANS (CO) transcription and the light-mediated stabilization of its encoded protein coordinately adjust photoperiodic flowering by triggering rhythmic expression of the floral integrator flowering locus T (FT). Diurnal accumulation of CO is modulated sequentially by distinct E3 ubiquitin ligases, allowing peak CO to occur in the late afternoon under long days. Here we show that CO abundance is not simply targeted by E3 enzymes but is also actively self-adjusted through dynamic interactions between two CO isoforms. Alternative splicing of CO produces two protein variants, the full-size COα and the truncated COß lacking DNA-binding affinity. Notably, COß, which is resistant to E3 enzymes, induces the interaction of COα with CO-destabilizing E3 enzymes but inhibits the association of COα with CO-stabilizing E3 ligase. These observations demonstrate that CO plays an active role in sustaining its diurnal accumulation dynamics during Arabidopsis photoperiodic flowering.

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