Abstract The remarkable plasticity of the biochemical machinery in plants allows the integration of a multitude of stimuli, enabling acclimation to a wide range of growth conditions. The integration of information on light and temperature enables plants to sense seasonal changes and adjust growth, defense, and transition to flowering according to the prevailing conditions. By now, the role of reactive oxygen species (ROS) as important signaling molecules has been established. Here, we review recent data on ROS as important components in the integration of light and temperature signaling by crosstalk with the circadian clock and calcium signaling. Furthermore, we highlight that different environmental conditions critically affect the interpretation of stress stimuli, and consequently defense mechanisms and stress outcome. For example, day length plays an important role in whether enhanced ROS production under stress conditions is directed towards activation of redox poising mechanisms or triggering programmed cell death (PCD). Furthermore, a mild increase in temperature can cause down-regulation of immunity and render plants more sensitive to biotrophic pathogens. Taken together, the evidence presented here demonstrates the complexity of signaling pathways and outline the importance of their correct interpretation in context with the given environmental conditions. Calcium, light signaling, photoperiod, programmed cell death, stress signaling, ROS, temperature Introduction Throughout their life cycle, plants are continuously exposed to changing environmental conditions. External stimuli perceived by the plant include changes in temperature, humidity, soil and air quality, and light. In nature, these factors are largely interdependent and therefore often change simultaneously. For example, during the daytime, temperatures are higher while humidity is lower as compared with the night. Similarly, in summer, light intensity is higher together with hotter weather than the rest of the year. In addition to abiotic factors, plants encounter biotic interactions with bacteria, fungi, and insects. While symbiotic interactions are beneficial, pathogen attack can be detrimental. Over the last several decades, researchers have aimed to define the term ‘stress’ (Selye, 1936; Lichtenthaler, 1998; Larcher, 2003; Kranner et al., 2010). Generally, plants are able to adjust to a wide range of different environmental conditions. However, once a certain threshold is exceeded, plants experience ‘stresses’. Some definitions of stress differentiate ‘eustress’, which is challenging for the organism but will lead to improved fitness, and ‘distress’, which exceeds the capacity for acclimation and causes irreversible damage or even death. Every stimulus can lead to eustress or distress. Intensity, amount, or a combination thereof are the determinants of the outcome, and the threshold is individual for each plant species (Gaspar et al., 2002). For example, plants experience continuous fluctuations in light intensity when leaves are shaded or exposed to the sun. Temperature and humidity changes happen on a daily basis and in a more extreme way on a seasonal basis. These stimuli can be considered as eustress, since plants are well adapted to these changes. In fact, many ‘stress signaling pathways’ that we are aiming to analyze are part of the plants’ intrinsic acclimation system to adjust to diurnal and seasonal changes. However, an intense stimulus under non-acclimated conditions may lead to distress. For example, plants activate cold defense pathways when days get shorter in autumn in anticipation of winter. Therefore, frost will have a different effect on the plant in summer as compared with late autumn. In other words, plants do not always respond to stimuli in the same way but in the context of the prevailing growth conditions (Janská et al., 2010). In this review, we highlight the remarkable plasticity of plant signaling networks discovered in the model plant Arabidopsis thaliana. Over the last years, an increasing number of studies have addressed the effects of different temperatures and light conditions on stress responses. Several important and well-known signaling molecules have been attributed ‘integrative’ signaling functions. Reactive oxygen species (ROS), together with calcium (Ca2+) and hormonal signaling appear to be at the center of the integration of multiple signals. ROS and the maintenance of cellular redox homeostasis ROS are highly reactive compounds and have been mainly considered as damaging agents over the years. Nowadays, the prevailing hypotheses describe ROS as key signaling components involved in a plethora of pathways. ROS formation and some of its signaling functions have recently been reviewed in depth by Waszczak et al. (2018) and Mittler et al. (2011). In brief, aerobic metabolism is inevitably accompanied by the production of ROS, including hydrogen peroxide (H2O2), hydroxyl radicals (·OH), superoxide radicals (O2−), and singlet oxygen (1O2). ROS formation is occurring continuously at the electron transport chains (ETCs) of photosynthesis in chloroplasts and respiration in mitochondria. Additionally, photorespiratory processes generate ROS in the peroxisomes. While intracellular ROS production is related to the activity of electron transport and metabolic events, extracellular ROS production in the apoplast is a process depending on a stimulus which activates ROS-producing enzymes such as apoplastic peroxidases, polyamine oxidases, and plasma membrane NADPH oxidases. To alleviate the potential damage of ROS to biomolecules, plants have developed a range of enzymatic as well as non-enzymatic ROS-scavenging mechanisms. Antioxidant proteins include superoxide dismutases, ascorbate peroxidases, and catalases. The most abundant cellular low molecular weight antioxidants are ascorbate and glutathione (GSH), which are interconnected by an oxidation–reduction cycle, termed the ‘Foyer–Asada–Halliwell’ cycle (Foyer and Noctor, 2011). It is important to emphasize that under optimal growth conditions, and even under stress conditions where ROS production is increased, the buffering capacity of the antioxidant machinery in the cell is typically not exceeded. The often used term ‘ROS accumulation’ refers to a spatially tightly controlled process, translating into changes in redox status of nearby (antioxidative) metabolites and proteins, thereby triggering signaling cascades necessary for cellular responses. Under severe stress conditions, cell death may be observed, which is, however, rarely a necrotic process, but mostly a form of programmed cell death (PCD), necessary to remobilize nutrients (Noctor and Foyer, 2016). Despite their simple chemical properties, high signal specificity can be obtained via ROS signaling. This specificity is obtained by compartmentation of ROS production and scavenging at different subcellular locations (Mignolet-Spruyt et al., 2016; Noctor and Foyer, 2016). Chloroplastic ROS production and subsequent signaling have been the center of attention regarding their importance in stress response. By acting as a central signaling hub regulating cellular metabolism, chloroplastic signaling plays a major role in determining plant fitness regarding abiotic as well as biotic factors (Kangasjärvi et al., 2014; Stael et al., 2015; Kmiecik et al., 2016). Changes in environmental conditions translate into changes in metabolism, including efficiency of photosynthesis and respiration, and consequently downstream anabolic and catabolic processes. Plants developed various means to optimize energy usage and maintenance of redox homeostasis. During light reactions of photosynthesis, ATP and NADPH are produced and provide energy and reducing power for many metabolic processes in the chloroplast, including keeping the antioxidant machinery in a reduced state. The hypothesis has been put forward that increases in the ATP/ADP and NADPH/NADP+ ratio would slow down electron transport in the photosynthetic electron transport chain (PET) causing its over-reduction and thereby enhancing ROS formation (Scheibe et al., 2005; Foyer et al., 2012). Such a situation may appear under stress conditions, when assimilatory, ATP- and NADPH-consuming processes are slowed down, and/or under abruptly increasing light intensity, when the PET and consequently the ADP/NADP+ pool is challenged with an additional amount of electrons. Consequently, the amount of ATP and NADPH that is generated needs to be re gulated accordingly and match downstream ADP and NADP+ regeneration reactions. An important mechanism to produce ATP without additional production of NADPH is non-photochemical quenching. Cyclic electron flow around PSI reduces the production of 1O2 and thereby protects PSII from photo-damage (Foyer et al., 2012). Additionally, it has been found that the ability to activate pathways that aid the regeneration of NADP+ improve plant fitness under stress conditions (Dghim et al., 2012). There are several NADP-dehydrogenases, which oxidize NADPH and thereby pass the electron on to another substrate, possibly even to another cellular compartment, to aid in metabolic processes. For example, a well-established process to shuttle excess electrons out of the chloroplast into the cytosol is the ‘malate valve’. Chloroplast-localized NADP-malate dehydrogenase (NADP-MDH) uses NADPH to convert oxaloacetate to malate, thereby regenerating NADP+ in the chloroplast. Malate is then transported into the cytosol and mitochondria, where it is converted back into oxaloacetate, thereby reducing one molecule of NAD+ which can be used in anabolic or catabolic processes (Scheibe, 2004). Interestingly, the malate valve is of particular importance for redox poising under stress conditions in short-day (SD)-grown plants, whereas long-day (LD)-grown plants rather employed ROS-scavenging mechanisms (such as up-regulation of ascorbate peroxidase and catalase) to counteract damage (Becker et al., 2006). The importance of day length for growth and stress defense will be elaborated on further in later paragraphs. Another metabolite used for electron shuttling is proline. Proline accumulates to high concentrations under a broad range of stress conditions (Szabados and Savouré, 2010; Verslues and Sharma, 2010; Rizzi et al., 2017), and its synthesis has been shown to be triggered by ROS production (Ben Rejeb et al., 2014, 2015). Stress-induced proline is mainly synthesized in chloroplasts (Székely et al., 2008). For each molecule of proline, two molecules of NADP+ are regenerated, thereby aiding in sustained electron flow through the PET. Proline accumulates during stress and is catabolized in the mitochondria after stress relief to provide electrons for respiratory processes during recovery (Hare and Cress, 1997; Szabados and Savouré, 2010). Given that stress-induced proline production functions as an electron shuttle from the chloroplast, it is not surprising that its biosynthesis is light dependent (Szabados et al., 1998; Abrahám et al., 2003). Proline content oscillates over the day–night cycle, with higher concentrations during the day than at night. In continuous darkness, these oscillations were abolished, suggesting that proline biosynthesis does not underlie the circadian clock but responds directly to the light input (Hayashi et al., 2000). Cellular ROS concentrations vary under different day lengths While it seems obvious that increasing amounts of light, and concomitant activity of the PET, lead to higher ROS production during the day as compared with the night, the day length also has a critical impact on cellular ROS production, as well as the resulting downstream signaling events. Importantly, photoperiod-regulated ROS signaling is not dependent on the total amount of light given during the day but solely on the number of hours per day that light is perceived (Queval et al., 2007). Despite the longer exposure to light in LDs as compared with SDs, ROS production has been found to be higher in SDs than in LDs. More specifically, the work of Michelet and Krieger-Liszkay (2012) reported higher superoxide and H2O2 production in SD-grown plants as compared with those grown in LDs. This increased ROS production partly originates from the chloroplastic PET. Additional studies on isolated thylakoids of SD-grown plants revealed higher superoxide production at PSI as compared with LD-grown plants, suggesting that PSI from SD thylakoids used O2 more efficiently as an electron acceptor than in LD thylakoids (Michelet and Krieger-Liszkay, 2012). Interestingly, it appears that NTRC, the chloroplast-localized isoform of NADPH-dependent thioredoxin reductase, is contributing to this effect, since ntrc plants did not show differences in ROS production under SD and LD conditions. NTRC is a bifunctional enzyme, harboring an NADPH-dependent thioredoxin reductase (NTR) domain and a C-terminal thioredoxin domain (TRX). NTRC delivers electrons from NADPH to TRX, which is then able to reduce downstream target proteins. The NADPH for this process is mainly produced through the oxidative pentose phosphate pathway (OPPP) in the night, in roots, or under stress conditions. Consequently, plants deficient in NTRC exhibited stunted growth, particularly under SDs (i.e. when nights were longer, when reducing reactions mediated by NTRC are of particular importance). ADP-glucose pyrophosphorylase (AGPase), an essential enzyme in starch biosynthesis, has been identified as one of the targets of NTRC, and growth defects in ntrc plants have been interpreted partly as an outcome of impaired starch synthesis. (Lepistö et al., 2009, 2013; Lepistö and Rintamäki, 2012). Furthermore, NTRC plays a major role in chlorophyll biosynthesis and the shikimate pathway in the shoots, root auxin biosynthesis, and lateral root formation. Since non-green plastids in the roots lack photosynthetic reactions, they depend on NADPH generated by the OPPP, and NTRC is proposed to play a major role in these tissues to maintain redox homeostasis (Kirchsteiger et al., 2012; Ferrández et al., 2012). Recent research has shown that not only the PET but also the mitochondrial ETC contributes to altered photoperiod-dependent ROS production (Pétriacq et al., 2017). Mutations in components of the mitochondrial complex I causes improper complex I assembly and result in a number of alterations regarding ROS production and redox homeostasis in mutant plants: complex I mutants exhibited differences in ROS concentration during the day and at the end of the night, NAD(H) content was higher under SDs and did not adjust upon shifting to LDs, and alternative oxidase content was higher and activity was enhanced. Mutant plants showed growth retardation particularly under SD conditions and impaired growth acceleration upon shift from SDs to LDs, caused by a lack of proper adjustment of carbon and nitrogen metabolism. This study suggests that mitochondrial complex I is necessary for proper growth acclimation to different light conditions. As previously stated, plants have developed sophisticated means for ROS detoxification and repair mechanisms to cope with sudden as well as prolonged changes in ROS production. Adaptations to protein repair and antioxidant machineries, described in the following studies, support the notion that plants grown in SDs have an altered ‘ROS profile’ as compared with LD plants. (i) The work of Bechtold et al. (2004) showed that there seems to be higher protein oxidation under SD conditions. The peptide methionine sulfoxide reductase 2 (PMSR2) is an important enzyme to repair protein damage caused by methionine oxidation. Particularly under SD conditions, loss of PMSR2 led to higher de novo protein synthesis. The resulting increase in energy demand enhanced respiration, and increased ROS production and concomitant oxidative pressure on the system, resulting in stunted growth. This phenotype was not observed under LD conditions. (ii) The mitochondrial ATP-dependent metalloprotease AtFtsH4, a key enzyme in quality control of membrane proteins, plays an important role in organelle development and leaf morphology, particularly under short photoperiods. While atftsh4 plants developed similarly to the wild type under LD conditions, in SDs they exhibited growth defects that correlated with enhanced ROS production and an increased number of carbonylated mitochondrial proteins (Gibala et al., 2009). (iii) The plastidial ATP/ADP transporters AtNTT1 and 2 are particularly important to regulate ATP import into the chloroplast at night for nocturnal metabolic activities and to prevent oxidative damage. Plants lacking AtNTT1 and 2 showed stunted growth together with increased ROS production and spontaneous lesion formation under SDs, while in LDs their phenotype was indistinguishable from that of the wild type (Reinhold et al., 2007). Circadian rhythm, the circadian clock, and ROS: ROS underlies diurnal cycling The metabolic connection between irradiation and ROS production is indisputable. Consequently, there are circadian effects on ROS metabolism, and significant inter-relationships between the circadian clock and ROS signaling have been reported (Karapetyan and Dong, 2018). The presence of a circadian clock is ubiquitous among all life on Earth, and is synchronized by the rotation of the planet. In all kingdoms of life, the circadian clock revolves around so-called ‘transcription–translation feedback loops’ (TTFLs). While this principle is the same in all circadian clocks, the components are not conserved among life forms. Briefly, in the model plant Arabidopsis thaliana, the morning-phased genes LATE ELONGATED HYPOCOTYL (LHY) and CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) activate the daytime-expressed PSEUDO-RESPONSE REGULATOR genes PRR7 and PRR9, which in turn repress LHY/CCA1, thereby allowing expression of the evening-expressed genes, including TIMING OF CAB EXPRESSION 1 (TOC1) and the evening complex EARLY FLOWERING 3 (ELF3)/ELF4/LUX ARRHYTHMO (LUX). This very simplified model is refined by many more regulators affecting timing of gene expression, and RNA as well as protein stability of the individual components. For a more detailed model of the Arabidopsis circadian clock, please see Hsu and Harmer (2014). The circadian clock is entrained by light perceived by phytochromes (red and far-red light receptors), cryptochromes (blue light receptors), and temperature. The circadian clock is involved in the regulation of almost all aspects of a plant’s life: growth, metabolism, flowering, abiotic stress defense, and immunity (Greenham and McClung, 2015). Hence, disturbance of the circadian clock leads to a number of cellular misregulations, including compromised plant fitness (Grundy et al., 2015). In addition to the TTFL clock, there is a parallel, non-transcriptional oscillating system conserved in all domains of life: the oxidation status of peroxiredoxins. Edgar et al. (2012) showed that diurnal over- and hyperoxidation of peroxiredoxins follows light/dark cycles. While the presence of a TTFL-based clock makes the peroxiredoxin rhythm dispensable for timekeeping, this redox cycle reflects the rhythmic generation of ROS through oxygen consumption during the day and therefore was suggested to be the ancient form of a circadian clock from which the TTFL type of clock evolved (Edgar et al., 2012). It has become evident that the redox rhythm-based and the TTFL-based clocks strongly influence each other. However, we are just beginning to understand the details of how the two systems are linked at a molecular level, and where the advantage of having two oscillatory systems resides. The core clock genes CCA1 and LHY appear to be particularly important in maintaining diurnal redox homeostasis. Interference with proper circadian expression of these genes affects cellular ROS concentrations as well as catalase activity, and consequently renders plants more sensitive under stress conditions (Lai et al., 2012). Conversely, it has been found that the redox-regulated transcriptional regulator NPR1 (NON-EXPRESSOR OF PATHOGENESIS-RELATED GENE 1), a core element in immune responses, regulates not only defense gene expression upon activation, but also expression of circadian clock genes. When the redox homeostasis is disturbed due to pathogen attack, NPR1 re-enforces the circadian clock by targeting morning as well as evening clock genes, and thereby ensures proper responsiveness to environmental stimuli without compromising immune responses (Zhou et al., 2015). Circadian rhythm and calcium concentrations Similar to ROS, calcium (Ca2+) is a multifaceted cellular signaling compound that responds to a multitude of stimuli. It has been implicated in the regulation of developmental processes as well as biotic and abiotic stress responses, and often acts in concert with ROS signaling (Steinhorst and Kudla, 2014; Niu and Liao, 2016). Ca2+ can stimulate ROS production by activation of NADPH-oxidases (Steinhorst and Kudla, 2014), and can also reduce cellular H2O2 concentrations by stimulating catalases (Yang and Poovaiah, 2002). Furthermore, Ca2+ is able to act directly on photosynthetic components in the chloroplast thylakoids, and thereby regulates photosynthetic efficiency, and consequently is able to affect ROS production by the PET and resulting redox conditions (Hochmal et al., 2015). In turn, ROS signals also affect Ca2+ concentrations; for example, exposure of plants to ozone (an air pollutant that triggers ROS production) triggers Ca2+ signaling. Interestingly, the Ca2+ signals differed between different experimental set-ups of ozone exposure, and could be clearly differentiated from H2O2 treatment (Evans et al., 2005), highlighting the potential in specificity of Ca2+ signaling. High cytosolic free Ca2+ concentrations ([Ca2+]cyt) are toxic to biomolecules (due to precipitation of phosphates, proteins, and DNA), and would cause constitutive activation of Ca2+ signaling components. Therefore, [Ca2+]cyt are kept low (at ~100 nM), whereas high concentrations are present in the apoplast, chloroplast, vacuole, and endoplasmic reticulum (ER), with concentrations up to several millimolar (Stael et al., 2012). Upon external stimuli, Ca2+ is released into the cytosol, causing a short-term (15 s to 20 min) increase in [Ca2+]cyt which is unique in terms of its spatio-temporal characteristic. This so-called ‘Ca2+ signature’ is able to confer specificity in triggering signaling cascades (McAinsh and Hetherington, 1998; McAinsh and Pittman, 2009). Interestingly, besides short-term signal-induced Ca2+ peaks, [Ca2+]cyt is subjected to circadian oscillation that is regulated by light and the circadian clock. It has been found that in addition to the TTFL-based and PRX-linked parts of the circadian clock, cytosolic cyclic ADP ribose (cADPR) and Ca2+ form an additional feedback loop (Dodd et al., 2007; Robertson et al., 2009). Similar to the mammalian system, cADPR acts as a trigger to release Ca2+ from the vacuole and the ER into the cytosol. In turn, cADPR content is regulated by the TTFL clock, and inhibition of cADPR production abolishes circadian oscillation of [Ca2+]cyt. Additionally, circadian [Ca2+]cyt oscillations are regulated by light. Red light promotes a rise in Ca2+ content during the day, and blue light is required for the decrease in the afternoon. The core clock component CCA1 determines the shape, phase, and amplitude of the Ca2+ oscillation (Xu et al., 2007; Dalchau et al., 2010). The light regime that plants are entrained to, namely photoperiod and light intensity, is contributing to the shape of diurnal Ca2+ oscillations (Love et al., 2004). In plants grown under LD conditions, Ca2+ peaks later after dawn (8 h) as compared with plants grown under SD conditions (4 h). Additionally, shorter photoperiods result in sharper Ca2+ curves with higher amplitudes, whereas oscillations were almost absent under very long photoperiods (20 h of light). Similarly, increasing light intensities led to an increase in the amplitude of oscillation. The involvement of Ca2+ in transmitting information on time is a process found not only in plants but also in mammals (Honma and Honma, 2003; Dodd et al., 2005). In plants, time monitoring by [Ca2+]cyt has been suggested to impact stomatal closure, stress response, and flowering time. For example, it has been shown that Ca2+-based signaling in response to cold was modulated by the time of the day and gated by the circadian clock (Dodd et al., 2006). The circadian modulation of low temperature-induced [Ca2+]cyt signals correlated to the circadian expression pattern of RD29A induction, a well-known gene in cold response. Additionally, low temperature-induced [Ca2+]cyt signals were significantly higher during the mid-photoperiod than at the beginning or end. Stimulus-induced changes in [Ca2+]cyt are closely monitored by a large number of Ca2+-sensing proteins, such as calmodulin (CaM), calmodulin-like proteins (CMLs), Ca2+-dependent protein kinases (CDPKs), calcineurin B-like proteins (CBLs) and their interacting kinases (CIPKs), syntaxins, and ion channels, and interact directly with transcription factors, to couple stimuli with responses (Hirschi, 2004; Hashimoto and Kudla, 2011). Despite the increasing knowledge on Ca2+ signaling and perception, it is not yet known by which mechanisms the diurnal Ca2+ oscillations are monitored and by which means these oscillations are integrated with short-term Ca2+ peaks upon specific stimuli (Dodd et al., 2005). Light versus temperature sensing in the control of growth and defense Light, as the primary energy source for plants, governs the main processes of nutrition and development, including carbohydrate fixation, nitrogen assimilation, and amino acid biosynthesis. Light conditions may vary in terms of quality (wavelength) or quantity (either intensity or photoperiod). Consequently, there is a requirement for strict regulation and acclimation of metabolic processes to the prevailing light conditions. For example, due to seasonal changes, plants have to adjust to a wide variety of day lengths. By adjusting the rates of photosynthesis, starch biosynthesis, and nitrogen assimilation, plants are able to acclimate to photoperiods as short as 3 h without showing any signs of starvation (Gibon et al., 2009). In addition to its metabolic function through photosynthesis, light is an important signaling component that is perceived by a large variety of photoreceptors and governs a multitude of processes in plant growth and development, including germination, phototropism, transition to flowering, stomatal conductance, and shade avoidance (Galvão and Fankhauser, 2015). Changes in temperature can range between high and low extremes, heat or freezing, which naturally is challenging and requires specific acclimatory processes. However, even small changes within the ambient temperature range (from ~15 °C to 28 °C in the temperate climate zone) have a significant impact on transcription, metabolism, and physiological acclimation. Morphological changes to elevated temperatures include hypocotyl and petiole elongation, leaf hyponasty, and premature flowering. These physiological adaptations are collectively termed thermomorphogenesis and have high similarity to ‘shade avoidance’ mechanisms (Gray et al., 1998; Koini et al., 2009). As light and temperature are the most important factors by which plants can sense daily and seasonal changes, there often is correlation between the two, and some perception and signaling components are shared (Casal and Qüesta, 2017; Legris et al., 2017). For example, the red light photoreceptor phytochrome B (PhyB) is a central component in the integration of light and temperature signaling (Fig. 1; Jung et al., 2016; Legris et al., 2016; Burgie et al., 2017). In brief, the inactive PhyB–Pr dimer is activated by the perception of red light during the day. Active PhyB–Pfr is inactivated by far-red light (e.g. during shading) and also by high temperature in a process called ‘dark’ or ‘thermal reversion’, after which it will again require light to re-activate PhyB–Pr. Therefore, the higher the temperatures, the more light is required to keep PhyB–Pfr in its activated state than at lower temperatures. The ratio of inactive, semi-activated, or fully active PhyB dimers enables the plant to sense temperature and light conditions simultaneously via PhyB. Further components that are involved in this sensing network include the other phytochromes (PhyA–E), the UV-B sensor UVR8, and the blue light receptor ZEITLUPE (ZTL). Fig. 1. View largeDownload slide Sensing of light and temperature by PhyB and downstream signaling. PhyB is activated by red light and inactivated by far-red light and dark/thermal reversion. PIF proteins regulate gene transcription and their activity is regulated by stability and protein interaction, including interaction with PhyB–Pfr. Active PhyB–Pfr destabilizes PIF proteins during the day. PIF4, a central regulator of growth and defense, is differentially regulated under LD and SD conditions, and integrates information on temperature and day length through interaction with PhyB–Pfr. For details, please see the text. PIF1/PIF3 are stabilized at night and repress ROS-related genes. HY5/HYH antagonize PIF1/PIF3 and are stabilized during the day when PIF1/PIF3 are degraded. HY5/HYH enhance ROS-related gene transcription in the light. Additionally, HY5 regulates cold tolerance in the dark and in the light in response to low temperatures. Cold response is further regulated by the TF CAMTA3. Additionally, CAMTA3 interacts with SA signaling. Fig. 1. View largeDownload slide Sensing of light and temperature by PhyB and downstream signaling. PhyB is activated by red light and inactivated by far-red light and dark/thermal reversion. PIF proteins regulate gene transcription and their activity is regulated by stability and protein interaction, including interaction with PhyB–Pfr. Active PhyB–Pfr destabilizes PIF proteins during the day. PIF4, a central regulator of growth and defense, is differentially regulated under LD and SD conditions, and integrates information on temperature and day length through interaction with PhyB–Pfr. For details, please see the text. PIF1/PIF3 are stabilized at night and repress ROS-related genes. HY5/HYH antagonize PIF1/PIF3 and are stabilized during the day when PIF1/PIF3 are degraded. HY5/HYH enhance ROS-related gene transcription in the light. Additionally, HY5 regulates cold tolerance in the dark and in the light in response to low temperatures. Cold response is further regulated by the TF CAMTA3. Additionally, CAMTA3 interacts with SA signaling. Figure 1 describes how the photoreceptor PhyB and downstream signaling components integrate information on light and temperature, and regulate ROS signaling, flowering, growth, and defense responses accordingly. Upon activation, PhyB–Pfr translocates from the cytosol into the nucleus, where it interacts with phytochrome-interacting factors (PIFs) (Pham et al., 2018). PIFs are transcription factors (TFs) with central functions in regulating the integration of light signals with hormonal signals, ROS signaling, developmental processes, and stress responses. PIFs can have a repressive or enhancing effect on target gene transcription, and are regulated by stability/abundance and protein interaction. For example, a genome-wide study revealed that PIF1 and PIF3 directly bound to promotors of several genes involved in ROS signaling and redox homeostasis (Chen et al., 2013). The TF ELONGATED HYPOCOTYL 5 (HY5) is a well-known positive regulator of light signaling and is involved in a plethora of cellular processes (Gangappa and Botto, 2016). HY5 and its homolog HYH are able to bind to the same promotor regions as PIF1/PIF3, thereby competing for transcriptional regulation of the same downstream target genes. PIF1/PIF3 were stabilized during the night and suppressed ROS signaling. Activated PhyB–Pfr during the day destabilized PIF1/PIF3, and HY5/HYH was stabilized, enhancing the transcription of ROS signaling genes (Chen et al., 2013). Furthermore, HY5 is an important TF in the establishment of cold tolerance. Cold conditions (4 °C) lead to stabilization of HY5, particularly at night, whereas HY5-dependent cold responses to cool ambient temperatures (17 °C) required light (Catala et al., 2011; Toledo-Ortiz et al., 2014). Another important PIF protein is PIF4, which emerged as a central regulator of plant growth, immunity, and abiotic stress tolerance (Quint et al., 2016). Downstream processes regulated by the PhyB–PIF4 signaling network include photoperiod perception, thermomorphogenesis, flowering, cold tolerance, and immunity. PIF4 transcription and protein abundance are strictly regulated by the circadian clock, temperature, and light conditions (Fig. 1; Nozue et al., 2007; Lee and Thomashow, 2012; Nomoto et al., 2012). Under SD conditions, PIF4 transcription was induced before dawn, leading to PIF4 accumulation and activity at the end of the night, which promoted growth induction (e.g. hypocotyl elongation). During the day, activated PhyB–Pfr bound to PIF4, resulting in PIF4 degradation. In contrast, under LD conditions, PIF4 was suppressed by the evening complex of the circadian clock at night, and is therefore exclusively expressed during the day. Furthermore, the active PhyB–Pfr–PIF4 complex was stabilized during the day by as yet unknown mechanisms, promoting growth and suppressing immunity (Lee and Thomashow, 2012). Consistently, Gangappa et al. (2017) showed that pif4 mutants showed enhanced disease tolerance and that defense-related genes were up-regulated, whereas overexpressors of PIF4 were more susceptible to stress. Additionally, the PhyB–PIF4 signaling network transmits photoperiod information to regulated cold/drought responses via the dehydration-responsive element-binding (DREB) protein/C-repeat binding factors (CBFs) (CBF1, CBF2, and CBF3; Fig. 1). CBF1–CBF3 are transcription factors that target >100 stress-responsive genes (collectively termed the ‘CBF regulon’) and induce tolerance to cold and drought (Akhtar et al., 2012). Stabilized PIF4 under LD conditions and warm (28 °C) SD conditions (see below) repressed CBF transcription. SDs and cool temperatures cause the destabilization of PIF4, thereby releasing the repression of and activating the CBF regulon (Lee and Thomashow, 2012). Suppression of the CBF regulon at warm temperatures and under LDs allows the direction of energy resources towards growth rather than cold/drought defense. Shortening days indicate the approach of colder temperatures, enabling plants to up-regulate the CBF regulon in anticipation of winter. The transition to flowering is an important step in plant development and is regulated by different mechanisms to ensure successful reproduction (Srikanth and Schmid, 2011; Cho et al., 2017). Light regulates the transition to flowering via the photoperiod pathway once day length exceeds 12 h. However, an increase of temperature (from 23 °C to 27 °C) under SD conditions is as effective in inducing flowering as a shift from SD to LD conditions (Balasubramanian et al., 2006). Temperature-induced flowering is triggered by PIF4 stabilization due to thermal inactivation of PhyB–Pfr. The monothiol glutaredoxin GRXS17 was found to be a key regulatory component in temperature- and photoperiod-dependent redox regulation of various metabolic enzymes and signaling components. GRXS17 regulates meristem function and induction of flowering (Cheng et al., 2011; Knuesting et al., 2015). High temperatures promote GRXS17 translocation from the cytosol towards the nucleus (Wu et al., 2012) where it was able to interact with Nuclear Factor Y Subunit C11/Negative Cofactor 2a (NF-YC11/NC2a), possibly to relay a redox signal to the nucleus to alter transcription and regulate meristem function (Knuesting et al., 2015). Taken together, these examples show that despite the signal specificity that light signaling is able to transmit, temperature is able to over-ride the light signals and thereby affect developmental processes, growth, and immunity. The regulation of programmed cell death Under abiotic as well as biotic stress conditions, ROS production is enhanced in different cellular compartments (Choudhury et al., 2017). Apoplastic ROS production is an active process triggered in response to biotic as well as abiotic stimuli. Intracellular ROS production in chloroplasts, mitochondria, and peroxisomes is a passive process, which is enhanced in response to stress conditions. Increased photorespiration under stress conditions causes increased H2O2 production in the peroxisomes. While H2O2 is efficiently scavenged by catalase and other redox-maintenance mechanisms, increased ROS production under stress conditions acts as an important trigger for defense responses. PCD is an active process triggered by increased ROS production and serves to fight off biotrophic pathogens [hypersensitive response (HR) mechanisms], or to reallocate resources (early senescence) (van Doorn et al., 2011; Foyer and Noctor, 2016). Figure 2 depicts a simplified scheme of the molecular events leading to PCD and includes regulatory components, which modulate the induction of cell death according to different light conditions. Fig. 2. View largeDownload slide Regulation of PCD in response to different day lengths. Enhanced ROS production under stress conditions triggers an increase in GSH biosynthesis and shift of the GSH pool towards the oxidized state. Oxidation of the GSH pool enhances ICS1 and subsequent SA biosynthesis. High SA concentrations trigger PCD (thick arrow). Additionally, SA may inhibit catalase activity, which contributes to ROS accumulation and reinforces the PCD pathway. The day length is an important factor for regulation of the PCD pathway. Under LD conditions, redox perturbation of the GSH pool favors high SA biosynthesis (thick arrow) and PCD. Under SD conditions, the SA level remains moderate (thin arrow) and energy is directed towards redox homeostasis. PP2Ab'γ plays an important role in ROS signaling under LD and SD conditions. MIPS regulates biosynthesis of MI, a metabolite that suppresses the PCD pathway in healthy plants. Fig. 2. View largeDownload slide Regulation of PCD in response to different day lengths. Enhanced ROS production under stress conditions triggers an increase in GSH biosynthesis and shift of the GSH pool towards the oxidized state. Oxidation of the GSH pool enhances ICS1 and subsequent SA biosynthesis. High SA concentrations trigger PCD (thick arrow). Additionally, SA may inhibit catalase activity, which contributes to ROS accumulation and reinforces the PCD pathway. The day length is an important factor for regulation of the PCD pathway. Under LD conditions, redox perturbation of the GSH pool favors high SA biosynthesis (thick arrow) and PCD. Under SD conditions, the SA level remains moderate (thin arrow) and energy is directed towards redox homeostasis. PP2Ab'γ plays an important role in ROS signaling under LD and SD conditions. MIPS regulates biosynthesis of MI, a metabolite that suppresses the PCD pathway in healthy plants. The cell death program requires the involvement of salicylic acid (SA), as lack of stress-induced SA (in sid2 or NahG plants) inhibits PCD under otherwise permissive conditions (Chaouch et al., 2010). Interestingly, the recent re-discovery that SA can bind catalase (Fig. 2; Yuan et al., 2017) was proposed to cause down-regulation of catalase activity and consequently further enhance ROS accumulation, which in turn enhances SA production, eventually contributing to cell death. In addition to its central role in the regulation of PCD, SA is important to sustain redox homeostasis in the cell. The redox-balancing function of SA is particularly important in abiotic stress defense (Khan et al., 2015). However, while exogenous application of SA can rescue cellular redox perturbation, it may induce lesion formation (PCD) if in excess (Chaouch et al., 2010). How SA concentrations are monitored has not been established yet, but it appears that the amount and redox status of the glutathione pools play an important role: when cellular ROS production is increased, GSH production is enhanced as well (Fig. 2; Queval et al., 2009). Additionally, high ROS production leads to a shift of the GSH pool towards the oxidized state. Only when a certain threshold of GSH increase and oxidation is reached, will SA biosynthesis be enhanced and PCD induced (Dghim et al., 2013; Han et al., 2013). Consistently, inhibition of GSH biosynthesis antagonized SA-dependent PCD, even under enhanced ROS production in cat2 plants (Han et al., 2013). Interestingly, SA-dependent PCD is dependent on the activity of photoreceptors PhyA and PhyB (Genoud et al., 2002). While endogenous SA content was comparable in phyA/phyB double mutants, downstream signaling towards PCD was strictly dependent on light and phytochrome signaling, but not on the functionality of chloroplasts. The use of so-called ‘lesion mimic mutants’ (LMMs), which exhibit necrotic lesion formation without prior pathogen attack, has allowed very important insight into the mechanism of PCD and its regulation under different growth conditions (Bruggeman et al., 2015b). Mutant plants lacking CAT2 activity have been used extensively to study the role of high cellular ROS concentrations in PCD and its regulation by the photoperiod. The CAT2 isoform accounts for the majority of the cellular catalase activity. Consequently, loss of CAT2 hinders efficient scavenging of H2O2 and causes serious perturbance of the cellular redox state. Interestingly, cat2 plants exhibit a conditional light-dependent cell death phenotype (Queval et al., 2007). While the redox equilibrium is perturbed under both LD and SD conditions, ectopic cell death is only observed under LD growth conditions (Queval et al., 2007). The inability to scavenge H2O2 by catalase in cat2 plants caused an increase of the glutathione pool together with its oxidation, whereas no significant differences in ascorbate, NAD+/NADH, or NADP+/NADPH concentrations were observed. Remarkably, while the GSH pool was largely oxidized in cat2 under both LD and SD conditions, only under LD conditions was excess SA production induced and triggered PCD (Fig. 2; Queval et al., 2009). In contrast, under SD conditions, SA content was moderate, and plant defense was rather directed towards redox homeostasis (Queval et al., 2012). A key component in this SD response is the protein phosphatase A subunit PP2Ab'γ (Fig. 2; Li et al., 2014). The maintenance of redox homeostasis under SDs required PP2A activity, since introduction of the pp2ab'γ mutation in cat2 plants caused a large increase in SA concentration together with initiation of PCD even under SD conditions. Despite the fat that only a few direct targets of PP2A have been identified to date, it is apparent that PP2A plays an important role in interorganellar ROS communication, specifically in immunity and light acclimation (Rahikainen et al., 2016). Given the central role of SA in redox homeostasis and induction of PCD, its concentration needs to be tightly regulated. To date, most regulatory elements of SA concentration appear to be transcriptional regulators of isochorismate synthase 1 (ICS1), the rate-limiting enzyme in SA biosynthesis (Dempsey et al., 2011; Kim et al., 2013). Interestingly, it appears that the metabolite myo-inositol (MI) is able to suppress the expression of ICS1 (and consequently SA production and PCD) by an as yet unknown mechanism (Fig. 2). Experimentally, exogenous application of MI inhibited necrotic lesion formation as efficiently as the genetic removal of SA accumulation in ICS1-deficient sid2 plants (Meng et al., 2009; Chaouch and Noctor, 2010; Li et al., 2014). The polyol MI is synthesized from glucose-6-phosphate via MIPS (myo-inositol-1-phosphate synthase), the rate-limiting enzyme in this pathway, and accumulates upon stress. While MIPS1 is the main isoform present in most cell types and developmental stages (Donahue et al., 2010), MIPS2 can compensate for the loss of MIPS1 under certain circumstances (Bruggeman et al., 2015a). Plants deficient in MIPS1 activity exhibit a low MI concentration along with increased production of SA, resulting in necrotic lesion formation (Meng et al., 2009). Consistent with this observation, MIPS1 expression is down-regulated in response to pathogen infection, thereby releasing the suppression on SA accumulation and enabling PCD. Interestingly, the mips1 LMM phenotype is light conditional, and appears only under LD conditions. The exact mechanisms of how the MI pathway integrates light and ROS signals to regulate SA concentration and PCD via ICS1 are not clear yet. However, several lines of evidence suggest the following. (i) The PCD observed in mips1 may be induced by excess ROS production in the chloroplast. Indeed, a reduction of chlorophyll content abolished lesion formation in mips1 (Meng et al., 2009). (ii) It has been found that the MIPS pathway is under the control of the two light signaling regulators FAR-RED ELONGATED HYPOCOTYL3 (FHY3) and its homolog FAR RED IMPAIRED RESPONSE1 (FAR1) (Ma et al., 2016), which play an important role in growth and development (chloroplast division), light signal integration with the circadian clock, abscisic acid (ABA) signaling, UV-B response, and plant immunity. Similar to mips1, the fhy3 far1 double mutants are also conditional LMMs, exhibiting a light-sensitive cell death phenotype triggered by changes in ROS concentration. However, in contrast to mips1, the fhy3 far1 phenotype could be mitigated by lengthening of the photoperiod. This could be explained by higher cellular ROS concentration under short photoperiods (see earlier section). (ii) Analysis of the expression profiles of MIPS1 and MIPS2 revealed that while both genes show a comparable transcriptional peak 4 h after dawn under SD and LD conditions, only in LDs does MIPS1, but not MIPS2, show a second peak 12–16 h after dawn (Ma et al., 2016). It is tempting to speculate that this second peak is necessary to keep the MI concentration raised under LD conditions to prevent PCD. In the case of mips1 plants, MIPS2 can potentially compensate for the early peak but not the late peak of MIPS1, thereby not sustaining MI biosynthesis throughout the day and releasing the repression of cell death. Several LMMs react not only to different light conditions, but also to other environmental factors, such as temperature and humidity (Alcázar and Parker, 2011; Hua, 2013). The variety of different mutants with different, even sometimes contrasting, responses to changes in temperature and humidity suggest that the underlying mechanisms are diverse. One such mechanism involves temperature perception by R-genes, specifically the NB-LRR type of R-proteins. Mutations in R-genes lead to constitutive up-regulation of defense responses and therefore reduced growth or even cell death. SA is an important mediator in these processes, but does not constitute the primary regulator. The mechanism of temperature perception by R-genes may lie in alterations in localization and complex formation (Hua, 2013). However, the exact molecular mechanisms are so far not understood. The transcription factor CAMTA3 (CALMODULIN-BINDING TRANSCRIPTION ACTIVATION 3) was shown to link Ca2+ signaling with SA signaling in a temperature-dependent manner (Fig. 1; Du et al., 2009). Plants deficient in CAMTA3 exhibit stunted growth, enhanced leaf chlorosis, and lesion formation, caused by constitutively increased SA concentration. This LMM phenotype could be rescued by an increase in ambient temperature to 27 °C. CAMTA3 is a calmodulin-binding transcription activation (CAMTA) factor that suppresses SA biosynthesis in healthy plants (Fig. 2). CAMTA factors are able to bind directly to specific DNA-binding motifs within the promotor regions of ICS1, as well as other components in SA signaling (Kim et al., 2013). Binding of CAMTA via their N-terminal repression modules (NRMs) inhibits target gene transcription. Upon low temperature exposure (4 °C), CaM/Ca2+ bind to the C-terminus of CAMTA, which releases the suppression of the NRM on the SA-related target genes (Kim et al., 2017) (Fig. 1). The up-regulation of SA biosynthesis and signaling leads to increases in SA concentration and consequently to activation of immunity and repression of growth. However, the up-regulation of SA does not directly aid in cold tolerance. Simultaneously with the activation of SA genes, CAMTA also up-regulates the CBF regulon and other CBF-independent cold-regulated genes, which triggers cold protection responses. Recently, an interesting model has been put forward, in which the plant immune receptors DOMINANT SUPRESSOR OF CAMTA3 NUMBER 1 and 2 (DSC1 and DSC2) act concertedly with CAMTA3 and other SA-repressing immune regulators (Lolle et al., 2017). According to this model, DSC1/DSC2 act as guardians of those immune regulators and as the primary components that trigger spontaneous PCD. Further studies will be needed to clarify the mechanistic details of SA-related gene expression and consequent regulation of immunity. Concluding remarks The studies highlighted in this review demonstrate important connections between signaling pathways in light, temperature, and stress response. There are substantial differences between plants grown under different day lengths, including stress defense strategies. SD-grown plants contain higher cellular concentrations of ROS as compared with LD-grown plants, and consequently employ an enhanced protein repair and antioxidant machinery. In SDs, diurnal calcium oscillations are marked by high amplitude and sharp curves. Increased ROS production leads to activation of redox poising mechanisms, including the malate valve and activation of signaling pathways involving PP2A. In contrast, plants grown under LD conditions actively suppress immune responses in favor of growth. Under optimal growth conditions, they exhibit lower cellular ROS concentrations as compared with SD-grown plants, and diurnal calcium oscillations are marked by a reduction in amplitude and elongation of phase. Enhanced ROS production activates ROS-scavenging systems, including ascorbate peroxidase and catalases, or directly triggers PCD. This strategy enables a quick response to pathogen attack by simply removing suppression of cell death. Temperature is an important factor in signal integration and enables the plant to fine-tune responses. There is intensive crosstalk with light signaling and, under certain conditions, changes in temperature can even over-ride light signals (e.g. flower induction). This factor is of crucial importance, considering that in the process of climate change we are experiencing a continuous rise in temperature. An involvement of day length and temperature changes in cold/drought response as well as immunity has been demonstrated, and further mechanistic details and consequences are about to be explored. It is important to point out that most data generated on the day length effect on stress responses have been generated in Arabidopsis and other facultative LD plants, in which flowering is triggered when day lengths exceed 12 h. Consequently, the observed differences in stress defense reflect the characteristics of vegetative versus reproductive growth: during vegetative growth in SDs, plants direct their energy towards redox homeostasis and leaf tissue protection, in order to survive until environmental conditions permit flowering (=reproduction). Once day lengths exceed 12 h and floral transition is triggered, energy is directed predominantly towards seed production and less towards protection of leaf material. Consequently, day length-specific responses may differ in facultative SD plants (e.g. rice). Taken together, the effect of light conditions, such as day length, and changes in temperature on stress defense constitute core features determining the transferability of results from the lab to the field, and will play major roles in future studies towards crop improvement. Abbreviations: Abbreviations: [Ca2+]cyt cytosolic free Ca2+ concentration cADPR cyclic ADP ribose CBF C-repeat binding factor ETC electron transport chain HR hypersensitive response LD long day LMM lesion mimic mutant PCD programmed cell death PET photosynthetic electron transport chain ROS reactive oxygen species SA salicylic acid SD short day TTFL transcription–translation feedback loop. Acknowledgements We thank Dr Michael Wrzaczek, Dr Alexey Shapiguzov, Dr Mikael Brosché, and Dr Luis Morales for critical comments on the manuscript. The authors are members in the Centre of Excellence in the Molecular Biology of Primary Producers (2014–2019) funded by the Academy of Finland (decision #271832). The authors thank all colleagues in the CoE for their input. References Abrahám E , Rigó G , Székely G , Nagy R , Koncz C , Szabados L . 2003 . Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis . 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Journal of Experimental Botany – Oxford University Press
Published: Mar 5, 2018
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