Plant Thermosensors.

Plants are exposed to temperature conditions that fluctuate over different time scales, including those inherent to global warming. In the face of these variations, plants sense temperature to adjust their functions and minimize the negative consequences. Transcriptome responses underlie changes in growth, development, and biochemistry (thermomorphogenesis and acclimation to extreme temperatures). We are only beginning to understand temperature sensation by plants. Multiple thermosensors convey complementary temperature information to a given signaling network to control gene expression. Temperature-induced changes in protein or transcript structure and/or in the dynamics of biomolecular condensates are the core sensing mechanisms of known thermosensors, but temperature impinges on their activities via additional indirect pathways. The diversity of plant responses to temperature anticipates that many new thermosensors and eventually novel sensing mechanisms will be uncovered soon.

Eco-physiology of maize crops under combined stresses.

The yield of maize (Zea mays L.) crops depends on their ability to intercept sunlight throughout the growing cycle, transform this energy into biomass and allocate it to the kernels. Abiotic stresses affect these eco-physiological determinants, reducing crop grain yield below the potential of each environment. Here we analyse the impact of combined abiotic stresses, such as water restriction and nitrogen deficiency or water restriction and elevated temperatures. Crop yield depends on the product of kernel yield per plant and the number of plants per unit soil area, but increasing plant population density imposes a crowding stress that reduces yield per plant, even within the range that maximises crop yield per unit soil area. Therefore, we also analyse the impact of abiotic stresses under different plant densities. We show that the magnitude of the detrimental effects of two combined stresses on field-grown plants can be lower, similar or higher than the sum of the individual stresses. These patterns depend on the timing and intensity of each one of the combined stresses and on the effects of one of the stresses on the status of the resource whose limitation causes the other. The analysis of the eco-physiological determinants of crop yield is useful to guide and prioritise the rapidly progressing studies aimed at understanding the molecular mechanisms underlying plant responses to combined stresses.

Hysteresis in PHYTOCHROME-INTERACTING FACTOR 4 and EARLY-FLOWERING 3 dynamics dominates warm daytime memory in Arabidopsis.

Despite the identification of temperature sensors and downstream components involved in promoting stem growth by warm temperatures, when and how previous temperatures affect current plant growth remain unclear. Here we show that hypocotyl growth in Arabidopsis thaliana during the night responds not only to the current temperature but also to preceding daytime temperatures, revealing a short-term memory of previous conditions. Daytime temperature affected the levels of PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) and LONG HYPOCOTYL 5 (HY5) in the nucleus during the next night. These factors jointly accounted for the observed growth kinetics, whereas nighttime memory of prior daytime temperature was impaired in pif4 and hy5 mutants. PIF4 promoter activity largely accounted for the temperature-dependent changes in PIF4 protein levels. Notably, the decrease in PIF4 promoter activity triggered by cooling required a stronger temperature shift than the increase caused by warming, representing a typical hysteretic effect; this hysteretic pattern required EARLY-FLOWERING 3 (ELF3). Warm temperatures promoted the formation of nuclear condensates of ELF3 in hypocotyl cells during the afternoon but not in the morning. These nuclear speckles showed poor sensitivity to subsequent cooling. We conclude that ELF3 achieves hysteresis and drives the PIF4 promoter into the same behavior, enabling a short-term memory of daytime temperature conditions.

Shade avoidance in the context of climate change.

When exposed to changes in the light environment caused by neighboring vegetation, shade-avoiding plants modify their growth and/or developmental patterns to access more sunlight. In Arabidopsis (Arabidopsis thaliana), neighbor cues reduce the activity of the photosensory receptors phytochrome B (phyB) and cryptochrome 1, releasing photoreceptor repression imposed on PHYTOCHROME INTERACTING FACTORs (PIFs) and leading to transcriptional reprogramming. The phyB-PIF hub is at the core of all shade-avoidance responses, whilst other photosensory receptors and transcription factors contribute in a context-specific manner. CONSTITUTIVELY PHOTOMORPHOGENIC1 is a master regulator of this hub, indirectly stabilizing PIFs and targeting negative regulators of shade avoidance for degradation. Warm temperatures reduce the activity of phyB, which operates as a temperature sensor and further increases the activities of PIF4 and PIF7 by independent temperature sensing mechanisms. The signaling network controlling shade avoidance is not buffered against climate change; rather, it integrates information about shade, temperature, salinity, drought, and likely flooding. We, therefore, predict that climate change will exacerbate shade-induced growth responses in some regions of the planet while limiting the growth potential in others.

Temperature regulation of auxin-related gene expression and its implications for plant growth.

Twenty-five years ago, a seminal paper demonstrated that warm temperatures increase auxin levels to promote hypocotyl growth in Arabidopsis thaliana. Here we highlight recent advances in auxin-mediated thermomorphogenesis and identify unanswered questions. In the warmth, PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and PIF7 bind the YUCCA8 gene promoter and, in concert with histone modifications, enhance its expression to increase auxin synthesis in the cotyledons. Once transported to the hypocotyl, auxin promotes cell elongation. The meta-analysis of expression of auxin-related genes in seedlings exposed to temperatures ranging from cold to hot shows complex patterns of response. Changes in auxin only partially account for these responses. The expression of many SMALL AUXIN UP RNA (SAUR) genes reaches a maximum in the warmth, decreasing towards both temperature extremes in correlation with the rate of hypocotyl growth. Warm temperatures enhance primary root growth, the response requires auxin, and the hormone levels increase in the root tip but the impacts on cell division and cell expansion are not clear. A deeper understanding of auxin-mediated temperature control of plant architecture is necessary to face the challenge of global warming.

COP1 destabilizes DELLA proteins in Arabidopsis.

DELLA transcriptional regulators are central components in the control of plant growth responses to the environment. This control is considered to be mediated by changes in the metabolism of the hormones gibberellins (GAs), which promote the degradation of DELLAs. However, here we show that warm temperature or shade reduced the stability of a GA-insensitive DELLA allele in Arabidopsis thaliana Furthermore, the degradation of DELLA induced by the warmth preceded changes in GA levels and depended on the E3 ubiquitin ligase CONSTITUTIVELY PHOTOMORPHOGENIC1 (COP1). COP1 enhanced the degradation of normal and GA-insensitive DELLA alleles when coexpressed in Nicotiana benthamiana. DELLA proteins physically interacted with COP1 in yeast, mammalian, and plant cells. This interaction was enhanced by the COP1 complex partner SUPRESSOR OF phyA-105 1 (SPA1). The level of ubiquitination of DELLA was enhanced by COP1 and COP1 ubiquitinated DELLA proteins in vitro. We propose that DELLAs are destabilized not only by the canonical GA-dependent pathway but also by COP1 and that this control is relevant for growth responses to shade and warm temperature.

Phytochrome B and PCH1 protein dynamics store night temperature information.

Plants experience temperature fluctuations during the course of the daily cycle, and although stem growth responds rapidly to these changes we largely ignore whether there is a short-term memory of previous conditions. Here we show that nighttime temperatures affect the growth of the hypocotyl of Arabidopsis thaliana seedlings not only during the night but also during the subsequent photoperiod. Active phytochrome B (phyB) represses nighttime growth and warm temperatures reduce active phyB via thermal reversion. The function of PHOTOPERIODIC CONTROL OF HYPOCOTYL1 (PCH1) is to stabilise active phyB in nuclear bodies but, surprisingly, warmth reduces PCH1 gene expression and PCH1 stability. When phyB was active at the beginning of the night, warm night temperatures enhanced the levels of nuclear phyB and reduced hypocotyl growth rate during the following day. However, when end-of-day far-red light minimised phyB activity, warm night temperatures reduced the levels of nuclear phyB and enhanced the hypocotyl growth rate during the following day. This complex growth pattern was absent in the phyB mutant. We propose that temperature-induced changes in the levels of PCH1 and in the size of the physiologically relevant nuclear pool of phyB amplify the impact of phyB-mediated temperature sensing.

Functional convergence of growth responses to shade and warmth in Arabidopsis.

Shade and warmth promote the growth of the stem, but the degree of mechanistic convergence and functional association between these responses is not clear. We analysed the quantitative impact of mutations and natural genetic variation on the hypocotyl growth responses of Arabidopsis thaliana to shade and warmth, the relationship between the abundance of PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and growth stimulation by shade or warmth, the effects of both cues on the transcriptome and the consequences of warm temperature on carbon balance. Growth responses to shade and warmth showed strong genetic linkage and similar dependence on PIF4 levels. Temperature increased growth and phototropism even within a range where damage by extreme high temperatures is unlikely to occur in nature. Both cues enhanced the expression of growth-related genes and reduced the expression of photosynthetic genes. However, only warmth enhanced the expression of genes involved in responses to heat. Warm temperatures substantially increased the amount of light required to compensate for the daily carbon dioxide balance. We propose that the main ecological function of hypocotyl growth responses to warmth is to increase the access of shaded photosynthetic organs to light, which implies functional convergence with shade avoidance.

Low Blue Light Enhances Phototropism by Releasing Cryptochrome1-Mediated Inhibition of PIF4 Expression.

Shade-avoiding plants, including Arabidopsis (Arabidopsis thaliana), display a number of growth responses, such as elongation of stem-like structures and repositioning of leaves, elicited by shade cues, including a reduction in the blue and red portions of the solar spectrum and a low-red to far-red ratio. Shade also promotes phototropism of de-etiolated seedlings through repression of phytochrome B, presumably to enhance capture of unfiltered sunlight. Here we show that both low blue light and a low-red to far-red light ratio are required to rapidly enhance phototropism in Arabidopsis seedlings. However, prolonged low blue light treatments are sufficient to promote phototropism through reduced cryptochrome1 (cry1) activation. The enhanced phototropic response of cry1 mutants in the lab and in response to natural canopies depends on PHYTOCHROME INTERACTING FACTORs (PIFs). In favorable light conditions, cry1 limits the expression of PIF4, while in low blue light, PIF4 expression increases, which contributes to phototropic enhancement. The analysis of quantitative DII-Venus, an auxin signaling reporter, indicates that low blue light leads to enhanced auxin signaling in the hypocotyl and, upon phototropic stimulation, a steeper auxin signaling gradient across the hypocotyl. We conclude that phototropic enhancement by canopy shade results from the combined activities of phytochrome B and cry1 that converge on PIF regulation.

Artificial selection for grain yield has increased net CO2 exchange of the ear leaf in maize crops.

Identifying the physiological traits indirectly selected during the search for high-yielding maize hybrids is useful for guiding further improvements. To investigate such traits, in this study we focused on the critical period of kernel formation because kernel number is the main yield component affected by breeding. Our results show that breeding has increased the number of florets per ear and ear growth rate but not the vegetative shoot growth rate, suggesting localised effects around the ear. Consistent with this possibility, breeding has increased the net CO2 exchange of the ear leaf in field-grown crops grown at high population densities. This response is largely accounted for by increased light interception (which increases photosynthesis) and by reduced rates of respiration of the ear leaf in modern hybrids compared to older ones. Modern hybrids show increased ear-leaf area per unit leaf dry matter (specific leaf area), which accounts for the reduced respiratory load per unit leaf area. These observations are consistent with a model where the improved ear leaf CO2 exchange helps the additional florets produced by modern hybrids to survive the critical period of high susceptibility to stress and hence to produce kernels.

Rewiring of auxin signaling under persistent shade.

Light cues from neighboring vegetation rapidly initiate plant shade-avoidance responses. Despite our detailed knowledge of the early steps of this response, the molecular events under prolonged shade are largely unclear. Here we show that persistent neighbor cues reinforce growth responses in addition to promoting auxin-responsive gene expression in Arabidopsis and soybean. However, while the elevation of auxin levels is well established as an early event, in Arabidopsis, the response to prolonged shade occurs when auxin levels have declined to the prestimulation values. Remarkably, the sustained low activity of phytochrome B under prolonged shade led to (i) decreased levels of PHYTOCHROME INTERACTING FACTOR 4 (PIF4) in the cotyledons (the organs that supply auxin) along with increased levels in the vascular tissues of the stem, (ii) elevated expression of the PIF4 targets INDOLE-3-ACETIC ACID 19 (IAA19) and IAA29, which in turn reduced the expression of the growth-repressive IAA17 regulator, (iii) reduced abundance of AUXIN RESPONSE FACTOR 6, (iv) reduced expression of MIR393 and increased abundance of its targets, the auxin receptors, and (v) elevated auxin signaling as indicated by molecular markers. Mathematical and genetic analyses support the physiological role of this system-level rearrangement. We propose that prolonged shade rewires the connectivity between light and auxin signaling to sustain shade avoidance without enhanced auxin levels.

CONSTANS delays Arabidopsis flowering under short days.

Long days (LD) promote flowering of Arabidopsis thaliana compared with short days (SD) by activating the photoperiodic pathway. Here we show that growth under very-SD (3 h) or darkness (on sucrose) also accelerates flowering on a biological scale, indicating that SD actively repress flowering compared with very-SD. CONSTANS (CO) repressed flowering under SD, and the early flowering of co under SD required FLOWERING LOCUS T (FT). FT was expressed at a basal level in the leaves under SD, but these levels were not enhanced in co. This indicates that the action of CO in A. thaliana is not the mirror image of the action of its homologue in rice. In the apex, CO enhanced the expression of TERMINAL FLOWER 1 (TFL1) around the time when FT expression is important to promote flowering. Under SD, the tfl1 mutation was epistatic to co and in turn ft was epistatic to tfl1. These observations are consistent with the long-standing but not demonstrated model where CO can inhibit FT induction of flowering by affecting TFL1 expression.

Shade delays flowering in Medicago sativa.

Shade-intolerant plants respond to the decrease in the red (R) to far-red (FR) light ratio (R:FR) occurring under shade by elongating stems and petioles and by re-positioning leaves, in a race to outcompete neighbors for the sunlight resource. In some annual species, the shade avoidance syndrome (SAS) is accompanied by the early induction of flowering. Anticipated flowering is viewed as a strategy to set seeds before the resources become severely limiting. Little is known about the molecular mechanisms of SAS in perennial forage crops like alfalfa (Medicago sativa). To study SAS in alfalfa, we exposed alfalfa plants to simulated shade by supplementing with FR light. Low R:FR light produced a classical SAS, with increased internode and petiole lengths, but unexpectedly also with delayed flowering. To understand the molecular mechanisms involved in uncoupling SAS from early flowering, we used a transcriptomic approach. The SAS is likely to be mediated by increased expression of msPIF3 and msHB2 in low R:FR light. Constitutive expression of these genes in Arabidopsis led to SAS, including early flowering, strongly suggesting that their roles are conserved. Delayed flowering was likely to be mediated by the downregulation of msSPL3, which promotes flowering in both Arabidopsis and alfalfa. Shade-delayed flowering in alfalfa may be important to extend the vegetative phase under suboptimal light conditions, and thus assure the accumulation of reserves necessary to resume growth after the next season.

Shade avoidance responses become more aggressive in warm environments.

When exposed to neighbour cues, competitive plants increase stem growth to reduce the degree of current or future shade. The aim of this work is to investigate the impact of weather conditions on the magnitude of shade avoidance responses in Arabidopsis thaliana. We first generated a growth rate database under controlled conditions and elaborated a model that predicts daytime hypocotyl growth as a function of the activity of the main photosensory receptors (phytochromes A and B, cryptochromes 1 and 2) in combination with light and temperature inputs. We then incorporated the action of thermal amplitude to account for its effect on selected genotypes, which correlates with the dynamics of the growth-promoting transcription factor PHYTOCHROME-INTERACTING FACTOR 4. The model predicted growth rate in the field with reasonable accuracy. Thus, we used the model in combination with a worldwide data set of current and future whether conditions. The analysis predicted enhanced shade avoidance responses as a result of higher temperatures due to the geographical location or global warming. Irradiance and thermal amplitude had no effects. These trends were also observed for our local growth rate measurements. We conclude that, if water and nutrients do not become limiting, warm environments enhance the shade avoidance response.

Light-mediated self-organization of sunflower stands increases oil yield in the field.

Here, we show a unique crop response to intraspecific interference, whereby neighboring sunflower plants in a row avoid each other by growing toward a more favorable light environment and collectively increase production per unit land area. In high-density stands, a given plant inclined toward one side of the interrow space, and the immediate neighbors inclined in the opposite direction. This process started early as an incipient inclination of pioneer plants, and the arrangement propagated gradually as a "wave" of alternate inclination that persisted until maturity. Measurements and experimental manipulation of light spectral composition indicate that these responses are mediated by changes in the red/far-red ratio of the light, which is perceived by phytochrome. Cellular automata simulations reproduced the patterns of stem inclination in field experiments, supporting the proposition of self-organization of stand structure. Under high crop population densities (10 and 14 plants per m2), as yet unachievable in commercial farms with current hybrids due to lodging and diseases, self-organized crops yielded between 19 and 47% more oil than crops forced to remain erect.

Perception of Sunflecks by the UV-B Photoreceptor UV RESISTANCE LOCUS8.

Sunflecks, transient patches of light that penetrate through gaps in the canopy and transiently interrupt shade, are eco-physiologically and agriculturally important sources of energy for carbon gain, but our molecular understanding of how plant organs perceive and respond to sunflecks through photoreceptors remains limited. The UV-B photoreceptor UV RESISTANCE LOCUS8 (UVR8) is a recent addition to the list of plant photosensory receptors, and we have made considerable advances in our understanding of the physiology and molecular mechanisms of action of UVR8 and its signaling pathway. However, the function of UVR8 in the natural environment is poorly understood. Here, we show that the UVR8 dimer/monomer ratio responds quantitatively and reversibly to the intensity of sunflecks that interrupt shade in the field. Sunflecks reduced hypocotyl growth and increased CHALCONE SYNTHASE (CHS) and ELONGATED HYPOCOTYL5 gene expression and CHS protein abundance in wild-type Arabidopsis (Arabidopsis thaliana) seedlings, but the uvr8 mutant was impaired in these responses. UVR8 was also required for normal nuclear dynamics of CONSTITUTIVELY PHOTOMORPHOGENIC1. We propose that UVR8 plays an important role in the plant perception of and response to sunflecks.

Long-Day Photoperiod Enhances Jasmonic Acid-Related Plant Defense.

Agricultural crops are exposed to a range of daylengths, which act as important environmental cues for the control of developmental processes such as flowering. To explore the additional effects of daylength on plant function, we investigated the transcriptome of Arabidopsis (Arabidopsis thaliana) plants grown under short days (SD) and transferred to long days (LD). Compared with that under SD, the LD transcriptome was enriched in genes involved in jasmonic acid-dependent systemic resistance. Many of these genes exhibited impaired expression induction under LD in the phytochrome A (phyA), cryptochrome 1 (cry1), and cry2 triple photoreceptor mutant. Compared with that under SD, LD enhanced plant resistance to the necrotrophic fungus Botrytis cinerea This response was reduced in the phyA cry1 cry2 triple mutant, in the constitutive photomorphogenic1 (cop1) mutant, in the myc2 mutant, and in mutants impaired in DELLA function. Plants grown under SD had an increased nuclear abundance of COP1 and decreased DELLA abundance, the latter of which was dependent on COP1. We conclude that growth under LD enhances plant defense by reducing COP1 activity and enhancing DELLA abundance and MYC2 expression.

Phytochrome B dynamics departs from photoequilibrium in the field.

Vegetation shade is characterized by marked decreases in the red/far-red ratio and photosynthetic irradiance. The activity of phytochrome in the field has typically been described by its photoequilibrium, defined by the photochemical properties of the pigment in combination with the spectral distribution of the light. This approach represents an oversimplification because phytochrome B (phyB) activity depends not only on its photochemical reactions but also on its rates of synthesis, degradation, translocation to the nucleus, and thermal reversion. To account for these complex cellular reactions, we used a model to simulate phyB activity under a range of field conditions. The model provided values of phyB activity that in turn predicted hypocotyl growth in the field with reasonable accuracy. On the basis of these observations, we define two scenarios, one is under shade, in cloudy weather, at the extremes of the photoperiod or in the presence of rapid fluctuations of the light environment caused by wind-induced movements of the foliage, where phyB activity departs from photoequilibrium and becomes affected by irradiance and temperature in addition to the spectral distribution. The other scenario is under full sunlight, where phyB activity responds mainly to the spectral distribution of the light.

Perception and signalling of light and temperature cues in plants.

Light and temperature patterns are often correlated under natural plant growth conditions. In this review, we analyse the perception and signalling mechanisms shared by both these environmental cues and discuss the functional implications of their convergence to control plant growth. The first point of integration is the phytochrome B (phyB) receptor, which senses light and temperature. Downstream of phyB, the signalling core comprises two branches, one involving PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and the other CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) and ELONGATED HYPOCOTYL 5 (HY5). The dynamics of accumulation and/or localization of each of these core signalling components depend on light and temperature conditions. These pathways are connected through COP1, which enhances the activity of PIF4. The circadian clock modulates this circuit, since EARLY FLOWERING 3 (ELF3), an essential component of the evening complex (EC), represses expression of the PIF4 gene and PIF4 transcriptional activity. Phytochromes are probably not the only entry point of temperature into this network, but other sensors remain to be established. The sharing of mechanisms of action for two distinct environmental cues is to some extent unexpected, as it renders these responses mutually dependent. There are nonetheless many ecological contexts in which such a mutual influence could be beneficial.

Light and temperature cues: multitasking receptors and transcriptional integrators.

Contents Summary 1029 I. Introduction 1029 II. Convergence at the receptor 1030 III. Convergence at transcriptional hubs 1031 IV. Convergence involving clock components 1033 V. Conclusions 1033 Acknowledgements 1033 References 1033 SUMMARY: The combined information provided by light and temperature cues helps to optimise plant body architecture and physiology. Plants possess elaborate systems to sense and respond to these stimuli. Simultaneous perception of light and temperature by dual receptors such as phytochrome B and phototropin leads to immediate signalling convergence. Conversely, cue asynchronies initiate separate pathways and the information of the earliest cue is stored, awaiting the arrival of the later cue to control transcription. Storage mechanisms can involve changes in the activity of selected clock components or epigenetic modifications, depending on the time delay between cues (hours, days or several months). We propose a conceptual framework in which the mechanisms of integration relate to the timing of cue sensing.