Thermomorphogenesis is defined as the suite of morphological changes that together are likely to contribute to adaptive growth acclimation to usually elevated ambient temperature [1, 2]. While many details of warmth-induced signal transduction are still elusive, parallels to light signaling recently became obvious (reviewed in [3]). It involves photoreceptors that can also sense changes in ambient temperature [3-5] and act, for example, by repressing protein activity of the central integrator of temperature information PHYTOCHROME-INTERACTING FACTOR 4 (PIF4 [6]). In addition, PIF4 transcript accumulation is tightly controlled by the evening complex member EARLY FLOWERING 3 [7, 8]. According to the current understanding, PIF4 activates growth-promoting genes directly but also via inducing auxin biosynthesis and signaling, resulting in cell elongation. Based on a mutagenesis screen in the model plant Arabidopsis thaliana for mutants with defects in temperature-induced hypocotyl elongation, we show here that both PIF4 and auxin function depend on brassinosteroids. Genetic and pharmacological analyses place brassinosteroids downstream of PIF4 and auxin. We found that brassinosteroids act via the transcription factor BRASSINAZOLE RESISTANT 1 (BZR1), which accumulates in the nucleus at high temperature, where it induces expression of growth-promoting genes. Furthermore, we show that at elevated temperature BZR1 binds to the promoter of PIF4, inducing its expression. These findings suggest that BZR1 functions in an amplifying feedforward loop involved in PIF4 activation. Although numerous negative regulators of PIF4 have been described, we identify BZR1 here as a true temperature-dependent positive regulator of PIF4, acting as a major growth coordinator.

Plants have a remarkable capacity to adjust their growth and development to elevated ambient temperatures. Increased elongation growth of roots, hypocotyls, and petioles in warm temperatures are hallmarks of seedling thermomorphogenesis. In the last decade, significant progress has been made to identify the molecular signaling components regulating these growth responses. Increased ambient temperature utilizes diverse components of the light sensing and signal transduction network to trigger growth adjustments. However, it remains unknown whether temperature sensing and responses are universal processes that occur uniformly in all plant organs. Alternatively, temperature sensing may be confined to specific tissues or organs, which would require a systemic signal that mediates responses in distal parts of the plant. Here, we show that Arabidopsis (Arabidopsis thaliana) seedlings show organ-specific transcriptome responses to elevated temperatures and that thermomorphogenesis involves both autonomous and organ-interdependent temperature sensing and signaling. Seedling roots can sense and respond to temperature in a shoot-independent manner, whereas shoot temperature responses require both local and systemic processes. The induction of cell elongation in hypocotyls requires temperature sensing in cotyledons, followed by the generation of a mobile auxin signal. Subsequently, auxin travels to the hypocotyl, where it triggers local brassinosteroidinduced cell elongation in seedling stems, which depends upon a distinct, permissive temperature sensor in the hypocotyl.

Global warming is one of the most detrimental aspects of climate change, affecting plant growth and development across the entire life cycle. This Review explores how different stages of development are influenced by elevated temperature in both wild plants and crops. Starting from seed development and germination, global warming will influence morphological adjustments, termed thermomorphogenesis, and photosynthesis primarily during the vegetative phase, as well as flowering and reproductive development. Where applicable, we distinguish between moderately elevated temperatures that affect all stages of plant development and heat waves that often occur during the reproductive phase when they can have devastating consequences for fruit development. The parallel occurrence of elevated temperature with other abiotic and biotic stressors, particularly the combination of global warming and drought or increased pathogen pressure, will potentiate the challenges for both wild and cultivated plant species. The key components of the molecular networks underlying the physiological processes involved in thermal responses in the model plant Arabidopsis thaliana are highlighted. In crops, temperature-sensitive traits relevant for yield are illustrated for winter wheat (Triticum aestivum L.) and soybean (Glycine max L.), representing cultivated species adapted to temperate vs. warm climate zones, respectively. While the fate of wild plants depends on political agendas, plant breeding approaches informed by mechanistic understanding originating in basic science can enable the generation of climate change-resilient crops.