Philip A. Wigge

H2A.Z-Containing Nucleosomes Mediate the Thermosensory Response in Arabidopsis

Plants are highly sensitive to temperature and can perceive a difference of as little as 1 degrees C. How temperature is sensed and integrated in development is unknown. In a forward genetic screen in Arabidopsis, we have found that nucleosomes containing the alternative histone H2A.Z are essential to perceiving ambient temperature correctly. Genotypes deficient in incorporating H2A.Z into nucleosomes phenocopy warm grown plants, and show a striking constitutive warm temperature transcriptome. We show that nucleosomes containing H2A.Z display distinct responses to temperature in vivo, independently of transcription. Using purified nucleosomes, we are able to show that H2A.Z confers distinct DNA-unwrapping properties on nucleosomes, indicating a direct mechanism for the perception of temperature through DNA-nucleosome fluctuations. Our results show that H2A.Z-containing nucleosomes provide thermosensory information that is used to coordinate the ambient temperature transcriptome. We observe the same effect in budding yeast, indicating that this is an evolutionarily conserved mechanism.

Transcription factor PIF4 controls the thermosensory activation of flowering

Plant growth and development are strongly affected by small differences in temperature. Current climate change has already altered global plant phenology and distribution, and projected increases in temperature pose a significant challenge to agriculture. Despite the important role of temperature on plant development, the underlying pathways are unknown. It has previously been shown that thermal acceleration of flowering is dependent on the florigen, FLOWERING LOCUS T (FT). How this occurs is, however, not understood, because the major pathway known to upregulate FT, the photoperiod pathway, is not required for thermal acceleration of flowering. Here we demonstrate a direct mechanism by which increasing temperature causes the bHLH transcription factor PHYTOCHROME INTERACTING FACTOR4 (PIF4) to activate FT. Our findings provide a new understanding of how plants control their timing of reproduction in response to temperature. Flowering time is an important trait in crops as well as affecting the life cycles of pollinator species. A molecular understanding of how temperature affects flowering will be important for mitigating the effects of climate change.

PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature

At high ambient temperature, plants display dramatic stem elongation in an adaptive response to heat. This response is mediated by elevated levels of the phytohormone auxin and requires auxin biosynthesis, signaling, and transport pathways. The mechanisms by which higher temperature results in greater auxin accumulation are unknown, however. A basic helix-loop-helix transcription factor, PHYTOCHROME-INTERACTING FACTOR 4 (PIF4), is also required for hypocotyl elongation in response to high temperature. PIF4 also acts redundantly with its homolog, PIF5, to regulate diurnal growth rhythms and elongation responses to the threat of vegetative shade. PIF4 activity is reportedly limited in part by binding to both the basic helix-loop-helix protein LONG HYPOCOTYL IN FAR RED 1 and the DELLA family of growth-repressing proteins. Despite the importance of PIF4 in integrating multiple environmental signals, the mechanisms by which PIF4 controls growth are unknown. Here we demonstrate that PIF4 regulates levels of auxin and the expression of key auxin biosynthesis genes at high temperature. We also identify a family of SMALL AUXIN UP RNA (SAUR) genes that are expressed at high temperature in a PIF4-dependent manner and promote elongation growth. Taken together, our results demonstrate direct molecular links among PIF4, auxin, and elongation growth at high temperature.

Phytochromes function as thermosensors in Arabidopsis

Combining heat and light responses Plants integrate a variety of environmental signals to regulate growth patterns. Legris et al. and Jung et al. analyzed how the quality of light is interpreted through ambient temperature to regulate transcription and growth (see the Perspective by Halliday and Davis). The phytochromes responsible for reading the ratio of red to far-red light were also responsive to the small shifts in temperature that occur when dusk falls or when shade from neighboring plants cools the soil. Science, this issue p. 897, p. 886; see also p. 832 Red-light photoreceptors also act as temperature sensors in plants. Plants are responsive to temperature, and some species can distinguish differences of 1°C. In Arabidopsis, warmer temperature accelerates flowering and increases elongation growth (thermomorphogenesis). However, the mechanisms of temperature perception are largely unknown. We describe a major thermosensory role for the phytochromes (red light receptors) during the night. Phytochrome null plants display a constitutive warm-temperature response, and consistent with this, we show in this background that the warm-temperature transcriptome becomes derepressed at low temperatures. We found that phytochrome B (phyB) directly associates with the promoters of key target genes in a temperature-dependent manner. The rate of phyB inactivation is proportional to temperature in the dark, enabling phytochromes to function as thermal timers that integrate temperature information over the course of the night.

Phytochrome B integrates light and temperature signals in Arabidopsis

Combining heat and light responses Plants integrate a variety of environmental signals to regulate growth patterns. Legris et al. and Jung et al. analyzed how the quality of light is interpreted through ambient temperature to regulate transcription and growth (see the Perspective by Halliday and Davis). The phytochromes responsible for reading the ratio of red to far-red light were also responsive to the small shifts in temperature that occur when dusk falls or when shade from neighboring plants cools the soil. Science, this issue p. 897, p. 886; see also p. 832 Red-light photoreceptors also act as temperature sensors in plants. Ambient temperature regulates many aspects of plant growth and development, but its sensors are unknown. Here, we demonstrate that the phytochrome B (phyB) photoreceptor participates in temperature perception through its temperature-dependent reversion from the active Pfr state to the inactive Pr state. Increased rates of thermal reversion upon exposing Arabidopsis seedlings to warm environments reduce both the abundance of the biologically active Pfr-Pfr dimer pool of phyB and the size of the associated nuclear bodies, even in daylight. Mathematical analysis of stem growth for seedlings expressing wild-type phyB or thermally stable variants under various combinations of light and temperature revealed that phyB is physiologically responsive to both signals. We therefore propose that in addition to its photoreceptor functions, phyB is a temperature sensor in plants.

Interlocking Feedback Loops Govern the Dynamic Behavior of the Floral Transition in Arabidopsis

The floral transition is a key decision in the plant life cycle and under complex regulation. Using modeling and experimental approaches, this work determines a core network of hub activities that accounts for many of the properties of the floral switch. This network exhibits switching behavior and suggests the balance of FT and TFL1 is critical for controlling plant architecture. During flowering, primordia on the flanks of the shoot apical meristem are specified to form flowers instead of leaves. Like many plants, Arabidopsis thaliana integrates environmental and endogenous signals to control the timing of reproduction. To study the underlying regulatory logic of the floral transition, we used a combination of modeling and experiments to define a core gene regulatory network. We show that FLOWERING LOCUS T (FT) and TERMINAL FLOWER1 (TFL1) act through FD and FD PARALOG to regulate the transition. The major floral meristem identity gene LEAFY (LFY) directly activates FD, creating a positive feedback loop. This network predicts flowering behavior for different genotypes and displays key properties of the floral transition, such as signal integration and irreversibility. Furthermore, modeling suggests that the control of TFL1 is important to flexibly counterbalance incoming FT signals, allowing a pool of undifferentiated cells to be maintained despite strong differentiation signals in nearby cells. This regulatory system requires TFL1 expression to rise in proportion to the strength of the floral inductive signal. In this network, low initial levels of LFY or TFL1 expression are sufficient to tip the system into either a stable flowering or vegetative state upon floral induction.

FT, A Mobile Developmental Signal in Plants

Plants synchronise their flowering with the seasons to maximise reproductive fitness. While plants sense environmental conditions largely through the leaves, the developmental decision to flower occurs in the shoot apex, requiring the transmission of flowering information, sometimes over quite long distances. Interestingly, despite the enormous diversity of reproductive strategies and lifestyles of higher plants, a key component of this mobile flowering signal, or florigen, is contributed by a highly conserved gene: FLOWERING LOCUS T (FT). The FT gene encodes a small globular protein that is able to translocate from the leaves to the shoot apex through the phloem. Plants have evolved a variety of regulatory networks that control FT expression in response to diverse environmental signals, enabling flowering and other developmental responses to be seasonally timed. As well as playing a key role in flowering, recent discoveries indicate FT is also involved in other developmental processes in the plant, including dormancy and bud burst.

Molecular and genetic control of plant thermomorphogenesis

Temperature is a major factor governing the distribution and seasonal behaviour of plants. Being sessile, plants are highly responsive to small differences in temperature and adjust their growth and development accordingly. The suite of morphological and architectural changes induced by high ambient temperatures, below the heat-stress range, is collectively called thermomorphogenesis. Understanding the molecular genetic circuitries underlying thermomorphogenesis is particularly relevant in the context of climate change, as this knowledge will be key to rational breeding for thermo-tolerant crop varieties. Until recently, the fundamental mechanisms of temperature perception and signalling remained unknown. Our understanding of temperature signalling is now progressing, mainly by exploiting the model plant Arabidopsis thaliana. The transcription factor PHYTOCHROME INTERACTING FACTOR 4 (PIF4) has emerged as a critical player in regulating phytohormone levels and their activity. To control thermomorphogenesis, multiple regulatory circuits are in place to modulate PIF4 levels, activity and downstream mechanisms. Thermomorphogenesis is integrally governed by various light signalling pathways, the circadian clock, epigenetic mechanisms and chromatin-level regulation. In this Review, we summarize recent progress in the field and discuss how the emerging knowledge in Arabidopsis may be transferred to relevant crop systems.

ELF3 Controls Thermoresponsive Growth in Arabidopsis

Plant development is highly responsive to ambient temperature, and this trait has been linked to the ability of plants to adapt to climate change. The mechanisms by which natural populations modulate their thermoresponsiveness are not known. To address this, we surveyed Arabidopsis accessions for variation in thermal responsiveness of elongation growth and mapped the corresponding loci. We find that the transcriptional regulator EARLY FLOWERING3 (ELF3) controls elongation growth in response to temperature. Through a combination of modeling and experiments, we show that high temperature relieves the gating of growth at night, highlighting the importance of temperature-dependent repressors of growth. ELF3 gating of transcriptional targets responds rapidly and reversibly to changes in temperature. We show that the binding of ELF3 to target promoters is temperature dependent, suggesting a mechanism where temperature directly controls ELF3 activity.

Thermal stress effects on grain yield in Brachypodium distachyon occur via H2A.Z-nucleosomes

BackgroundCrop plants are highly sensitive to ambient temperature, with a 1 ºC difference in temperature sufficient to affect development and yield. Monocot crop plants are particularly vulnerable to higher temperatures during the reproductive and grain-filling phases. The molecular mechanisms by which temperature influences grain development are, however, unknown. In Arabidopsis thaliana, H2A.Z-nucleosomes coordinate transcriptional responses to higher temperature. We therefore investigated whether the effects of high temperature on grain development are mediated by H2A.Z-nucleosomes.ResultsWe have analyzed the thermal responses of the Pooid grass, Brachypodium distachyon, a model system for crops. We find that H2A.Z-nucleosome occupancy is more responsive to increases in ambient temperature in the reproductive tissue of developing grains compared withvegetative seedlings. This difference correlates with strong phenotypic responses of developing grain to increased temperature, including early maturity and reduced yield. Conversely, temperature has limited impact on the timing of transition from the vegetative to generative stage, with increased temperature unable to substitute for long photoperiod induction of flowering. RNAi silencing of components necessary for H2A.Z-nucleosome deposition is sufficient to phenocopythe effects of warmer temperature on grain development.ConclusionsH2A.Z-nucleosomes are important in coordinating the sensitivity of temperate grasses to increased temperature during grain development. Perturbing H2A.Z occupancy, through higher temperature or genetically, strongly reduces yield. Thus, we provide a molecular understanding of the pathways through which high temperature impacts on yield. These findings may be useful for breeding crops resilient to thermal stress.