Abstract
Low temperature is one of the major factors that adversely affect crop yields by causing restraints on plant growth and productivity. However, most temperate plants have the ability to acclimate to cooler temperatures. Cold acclimation is a process which increases the freezing tolerance of an organism after exposure to low, non-freezing temperatures. The main trigger is a decrease in temperature levels, but light reduction has also been shown to have an important impact on acquired tolerance. Since the lowest temperatures are commonly reached during the night hours in winter time and is an annually recurring event, a favorable trait for plants is the possibility of sensing an imminent cold period. Consequently, extensive crosstalk between light- and temperature signaling pathways has been demonstrated and in this review interesting interaction points that have been previously reported in the literature are highlighted.
Introduction
Plants are forced to adapt to the prevailing environment surrounding them, since they, in contrast to many other species, are unable to migrate to more favorable localities. Cold stress, which includes chilling (0–12°C) and/or freezing (<0°C) temperatures, can adversely affect crop yields by causing restraints on sowing time, extensive tissue damages and stunted growth.Citation1 However, most plants growing in temperate regions have evolved traits which make it possible for them to cope with freezing temperatures. This fitness advantage requires that the plant is first allowed to acclimate to cooler temperatures; in response to a mild cold stress a cascade of transcriptional, regulatory and metabolic reactions are triggered that greatly enhance the tolerance to later, more severe temperatures—a process known as cold acclimation.Citation2
The main trigger of the acclimation process is the low non-freezing temperatures, but light reduction has also been shown to have an important impact on acquired tolerance.Citation3 In natural environments, light and temperature reductions often occur in parallel, where the lowest temperatures are commonly reached during the night hours in winter time. Since low temperatures recur annually a favorable trait for a temperate plant is the possibility of sensing an imminent cold period, which can be utilized for optimizing the production of protective proteins. Moreover, since the hours of daylight decreases continuously before the upcoming winter, the shortening of the daily photoperiod is a strong indicator of the transition from summer to winter season and is therefore, in some aspects, a more reliable indicator than the actual temperature, which can be highly fluctuating on a daily basis.Citation4 Consequently, interplay between light and cold acclimation signaling pathways have been reported in the literature. In this short review interesting findings related to this subject are highlighted, with a focus on interactions between cold responses and the quality of light, the circadian clock and the photoperiod.
Cold Acclimation and Quality of Light
Light is one of the most important factors for plant development, by being a major energy source.Citation5 The development is affected by the amount of light received, the quality of that light (wavelength), the incident light and relative length of day and night. Light signals are an integrated ingredient in many various responses, e.g., shade avoidance and flower induction, and have been associated with other environmental stimuli, e.g., circadian rhythms and gravity signals. Light signals are perceived through different photoreceptors, phytochromes (PHYs), phototropins and cryptochromes (CRYs), which absorb different wavelengths.Citation5–Citation7 The PHYs mainly absorb red and far-red wavelengths, whereas CRYs and phototropins absorb blue and ultraviolet A (UVA) light, respectively.
In general, light has been shown to enhance the expression of cold regulated genes (CORs) in different plant species and phytochromes have been demonstrated to be important factors in the transcriptional control of CORs.Citation8–Citation13 During twilight (dusk and dawn) there is a decrease in the red and far-red wavelength ratio (R/FR), i.e., the red light decreases while the far-red light increases. Interestingly, several studies have shown that cold acclimation is dependent on available red and far-red light, since a red pulse given shortly after dark suppresses the acclimation in different woody species.Citation14–Citation16 However, this effect can be counteracted if a far-red light is given directly after the red pulse. Additionally, in the studies, it was shown that acclimation is promoted if a far-red light is given by the end-of-day.
Many of the COR genes in A. thaliana contain the Dehydration-Responsive/C-repeat Element (CRT/DRE element) in their promoter regions, which is a target for the C-repeat Binding Factors (CBFs) TFs that are known to have a prominent role in the acclimation process in this species.Citation17–Citation22 The CRT/DRE element was identified specifically in A. thaliana, but similar elements have since been shown to play similar roles in a number of plant species studied.Citation23–Citation25 In addition, the TFs zinc-finger protein ZAT12 and Related to ABI3/VP1 (RAV1) have also a role in the acclimation process in A. thaliana, and are induced in parallel and upstream of the CBFs,Citation26–Citation28 and where ZAT12 is likely to have a negative regulatory role of the CBFs.Citation26 Interestingly, Franklin and WhitelamCitation16 demonstrated that a low R/FR ratio increases the expression levels of the CBFs as well as COR genes in A. thaliana, and in phyB and phyD mutants grown under low R/FR and at 16°C the expression of COR15a was increased, indicating a negative role of these phytochromes on CBF target genes in a high R/FR light. However, the low R/FR ratio did not increase the expression levels of ZAT12 or RAV1. ZAT12 has been coupled to various abiotic stress conditionsCitation29,Citation30 and was originally identified as a light stress-response gene,Citation31 but shown to not be a necessity for obtaining cold tolerance (at 10°C) in A. thaliana.Citation29 This indicates that ZAT12 has a more prominent role in light signaling pathways than cold acclimation and that the low R/FR-mediated response is coupled specifically to the CBF regulon.
Conclusions have also been drawn that, in order for the acclimation process to proceed, the level of the activated Pfr form of the phytochromes must reach below a certain threshold.Citation15 Actually, any changes in the R/FR ratio are monitored as changes in the relative proportions of the in-active Pr and active Pfr forms of the phytochromes and this change is mainly monitored by PHYB.Citation7 This is interesting, since it indicates that PHYB is one of the prominent phytochromes involved in the stimulation of cold-induced gene expression.
Another interesting finding is the FIERY1 (FRY1/SAL1) gene in A. thaliana that encodes a bi-functional enzyme with 3′(2′),5′-bisphosphate nucleotidase and inositol polyphosphate 1-phosphatase activities, and where the latter is involved in the catabolism of the secondary messenger IP3.Citation32 The fiery1 mutant displays reduced ability to cold acclimate and sustained induction of cold regulated genes, such as CBF2 and COR47, due to higher accumulation of IP3.Citation33,Citation34 Consequently, FIERY1 is thought to be a negative regulator of cold induced genes, via the suppression of IP3 and thereby a decreased release of Ca2+ from internal stores. Recently, FIERY1 was shown to be regulated by light as well as attenuate light responses via its 3′(2′),5′-bisphosphate nucleotidase activity, in contrast to the inositol polyphosphate 1-phosphatase activity used in stress responses.Citation35 Moreover, the fiery1–6 mutant studied was hyper-sensitive to red, far-red as well as blue wavelengths.
Cold Acclimation and Circadian Rhythms
The circadian clock is a mechanism used by plants to determine the time of day and enables the organism to optimize biological activities with changes in the surrounding environment.Citation36–Citation38 Circadian signaling networks generate rhythms that maintain a periodicity close to 24 hours and these rhythms persist in continuous environmental conditions, e.g., continuous light, and display stability over a range of physiological temperatures. The rhythms are endogenously produced, but can be entrained by exogenous cues, so called Zeitgebers (ZTs), with the purpose of keeping the rhythms matched to changes in the external environment, e.g., a shortening of the photoperiod or decrease in temperature.
Since the lowest temperature and light levels occur during the night-hours species that can anticipate recurring night/day changes have an adaptive advantage.Citation39–Citation43 Many plants exhibit a temperature compensation, whereby the clock maintain robust and accurate in timing over different ambient temperatures.Citation44–Citation46 Different clock mutants have been identified that show loss of temperature compensation; the clock runs slightly faster at higher temperatures in these mutants.Citation47,Citation48 Indeed, cold as well as chilling tolerance has been shown to be regulated endogenously by the circadian clock;Citation49–Citation53 the amount of tolerance to low temperatures displays daily oscillations and is dependent on the time of exposure. The tolerance phase starts near dusk and last throughout most of the night. Consequently, survival is optimal when plants are exposed to cold near subjective dusk, which coincides with the peak in expression levels of many COR genes.
In contrast, Michael et al.Citation40 provided evidence of a clock in A. thaliana that is primarily sensitive to temperature and can act independently of light cues, demonstrating the existence of two distinguishable clocks. They also showed that genes can respond preferentially to one of the clocks, since the rhythm of Catalase 3 (CAT3) was more sensitive to temperature than light and vice versa for Chlorophyll A/B binding protein 2 (CAB2). Interestingly, N'Doye et al.Citation54 observed much earlier that the diurnal rhythmical variations of the polyamine levels in tomato (Lycopersicum esculentum Mill.cv. Ace 55) were primarily controlled by temperature cycles and to a lesser content by light. In addition, under normal diurnal conditions optimal stabilization of chloroplast membranes occurred in coincident with high polyamine levels during the night and low levels during the day.
The underlying transcriptional regulatory network (TRN) of the circadian clock is primarily light-driven, but can also be entrained by temperature.Citation55 The temperature-driven entrainment of the clock is currently poorly understood, although some pieces to the puzzle are the Pseudo-Response Regulator 5, 7 and 9 (PRR5, PRR7 and PRR9) genes, of which at least the two latter have been shown to be essential for temperature entrainment in A. thaliana.Citation56,Citation57 These genes function within the core of the clock TRN, but do not encode DNA-binding proteins and therefore probably do not directly regulate transcription.Citation57–Citation60 Recently, Nakamichi et al.Citation61 showed that the A. thaliana prr5–11 prr7–11 prr9–10 triple mutant (d975) have a higher tolerance to cold stress than WT when transferred directly to −5° in the dark. In this mutant several clock-associated genes are arrhythmically expressed, including the key regulators MYB-like Circadian Clock-Associated 1 (CCA1) and Late Elongated Hypocotyl (LHY) TFs. In addition, by a comparison to published microarray experiments, a major portion of the upregulated genes in d975 during warm temperatures in the late afternoon (ZT8–12) were identified as cold induced as well. For example, in their study, the CBF2–3 genes as well as three target genes of CBF3 had higher expressions levels in d975 than in WT and under cold stress the expression levels of CBF1 and CBF3 reached the same levels as in WT, whereas for CBF2 they were increased 2–3 times in d975. It was therefore suggested that PRR5, PRR7 and PRR9 dampens the CBFs during non-stress conditions.
In contrast, a dampening effect of genes participating in the core TRN, such as LHY, Timing of CAB expression 1 (TOC1), PRR3, PRR5, PRR7 and PRR9, as well as output genes from the clock, such as CCR1–2 and CAB2, during low temperatures in long-daylength conditions has been demonstrated in A. thaliana;Citation53,Citation62,Citation63 the genes display reduced low-amplitude cycles and are clamped to a steady expression level, while in continuous light they become fully arrhythmical. Moreover, in woody chestnut tree the PRR5, PRR7, PRR9, LHY and TOC1 genes display a similar response pattern as their counterparts in A. thaliana;Citation64,Citation65 during normal warm conditions they accumulate and oscillate in an analogous order, while during low temperature they are clamped to a steady expression level. However, in chestnut the cycles were shown to be fully diminished during a short- as well as long-daylength.
GIGANTEA (GI) is a protein that participates in the core of the clock TRN, but also plays important roles in phytochrome signaling and photoperiodic flowering (Fig. 2).Citation47,Citation59,Citation66,Citation67 Interestingly, Cao et al.Citation68 showed that GI in A. thaliana is induced by cold, but not salt, mannitol or abscisic acid, and that mutant gi-3 plants display decreased cold tolerance and impaired acclimation ability. However, there was no significant difference in transcript levels of the CBFs between WT plants and gi-3 mutants, indicating that GI mediates cold response via a CBF-independent pathway.
Several studies have demonstrated that many cold-regulated genes exhibit circadian changes in their expression levels at warm temperatures, and that TFs prominent in the response are gated by the circadian clock.Citation28,Citation53,Citation69 In Fowler et al.Citation28 it was shown that maximum increase in expression levels for the CBFs as well as RAV1 occurred when the specimens were exposed to 4°C in the early morning (ZT4) and, in contrast, near dusk (ZT16) for ZAT12. It was also demonstrated that the expression levels of the CBFs become arrhythmical in specimens constitutively expressing the core clock gene CCA1 during low temperatures, which indicate that a functional clock is required for the gating of these genes during cold stress. The gating of cold-responsive genes has also been demonstrated in chilling-sensitive tomato, which indicates that this mechanism is conserved among plants with various tolerances to low temperatures.Citation70–Citation72 In contrast, when the clock is resumed upon re-warming it is altered and out of phase in tomato.Citation70,Citation71 This arrest causes a mistiming of the activation of proteins and thereby a disruption in photosynthetic and cellular metabolism, and is thought to be a prominent contributor to the cold-intolerance in chilling-susceptible plants.
Cold Acclimation and Photoperiodism
Photoperiodism, i.e., the ability to sense seasonal changes in night length, is a mechanism used by plants to determine the time of year and thereby when it is time to flower or begin dormancy.Citation4 The photoperiod is estimated through the utilization of the phytochrome photoreceptor system and the circadian clock. Most woody plants are highly sensitive to the photoperiod and, furthermore, temperate woody plants have a much higher capacity to cold acclimate and tolerate extreme low temperatures than herbaceous plants.Citation73 It is now well-established that an acquired freezing tolerance is obtained by first a shortening of the photoperiod and thereafter a decrease in temperature.Citation74–Citation78 An exposure to a short photoperiod is not a prerequisite of frost hardening, but short days alone have been shown to induce cold tolerance in woody plants, however with a significantly lower hardening rate than freezing temperatures.
The additive effect of short daylength and low temperature has been established on the physiological, metabolic as well as the transcriptional regulatory level.Citation79–Citation83 For example, in aspen trees and Scots Pine LT50 (Lethal Temperature which 50% of the samples are dead) values occurred at significantly lower sub-zero temperatures when specimens were treated with a low temperature in combination with a short daylength than in combination with a long daylength. Puhakainen et al.Citation83 showed that the expression levels of the silver birch dehydrin Bplti36, which is plausibly under CBF control, increased substantially in response to low temperatures preceded by a short daylength exposure, but only moderately when exposed to a long daylength. Additionally, El Kayal et al.Citation81 showed that the expression of two CBF genes isolated from Eucalyptus gunnii accumulated to higher levels in response to low temperatures combined with a short daylength than to low temperatures under long days. Welling et al.Citation80 showed that short-days and low temperature can induce cold acclimation independently in aspen. But more interestingly, the dehydrin DSP16-like gene was shown to be regulated by the photoperiod via phyA during short-days, but at low temperatures it was regulated by a different mechanism, since in hybrid aspen overexpressing phyA the gene was strongly induced at low temperatures during short- as well as long-days.Citation84
The above described phenomenon seen in woody plants has also been observed in some herbaceous plant varieties.Citation85–Citation90 For example, the study by Alonso-Blanco et al.Citation86 showed that the sub-tropical A. thaliana variety CapeVerde Islands behaved similarly under both short and long daylength, whereas the overall lower freezing tolerant northern European variety Landsberg erecta showed a small increase in freezing tolerance when grown under short days. The similar has been observed for different barley varieties,Citation85 where a variety with a very low sensitivity to short daylength responded in a similar way to low temperatures during both long and short daylength treatments, whereas for the short daylength sensitive variety exposure to a short photoperiod resulted in an increased tolerance.
Since short days alone are not a prerequisite for acquiring cold tolerance these two environmental cues are believed to be regulated by distinct, although overlapping, pathways, which has also been indicated by several experimental studies.Citation79,Citation80,Citation86 The additive effect is clearly coupled to whether the plant is photoperiod sensitive or not, since varieties less sensitive to a short daylength respond similarly to low temperatures irrespective of a long or short daylength exposure and, in contrast, photoperiod-sensitive varieties exhibit an additive tolerance to low temperature that is preceded by an exposure to a short photoperiod.
Conclusions
For plants growing in temperate regions, light and temperature levels are two major environmental factors implicating development and survival. In such habitats, these two factors display extensive variation over the year, where lowest light and temperature levels occur during the night-hours in winter time. Consequently, plants that can link a decrease in daily photoperiod with an upcoming winter will obtain a longer time to prepare for a more extreme climate and should thereby lead to an adaptive advantage. Interestingly, the existence of multiple oscillators have been identified in many speciesCitation45,Citation55,Citation91–Citation93 and a light as well as a temperature clock in A. thaliana was suggested by Michael et al.Citation40, where the light driven clock functions during normal diurnal conditions but seems to be overridden by a low temperature clock when the levels drop below a certain point. Moreover, these oscillators do not function independently of each other, but are partially overlapping and redundant. This intricate mechanism provides plants with a flexible way to integrate light and temperature cycles, and with a highly dynamic response system against environmental changes, which can subsequently lead to an enhanced fitness. Cold acclimation should therefore not be studied as an isolated process, since it is highly integrated with pathways coupled to light reduction. We should therefore see more of research papers concerning crosstalk between light signaling, photoperiod, circadian clock and cold acclimation pathways in the future.
Abbreviations
| CORs | = | cold induced genes |
| PHYs | = | phytochromes |
| CRYs | = | cryptochromes |
| UVA | = | ultraviolet A |
| R/FR | = | red and far-red wavelength ratio |
| CRT/DRE | = | dehydration-responsive/C-repeat element |
| ZAT12 | = | zinc-finger protein |
| RAV1 | = | related to ABI3/VP1 |
| ZTs | = | zeitgebers |
| CAT3 | = | catalase 3 |
| CAB2 | = | chlorophyll A/B binding protein 2 |
| TRN | = | transcriptional regulatory network |
| PRR5 | = | pseudo-response regulator 5 |
| PRR7 | = | pseudo-response regulator 7 |
| PRR9 | = | pseudo-response regulator 9 |
| CCA1 | = | MYB-like circadian clock-associated 1 (CCA1) |
| LHY | = | late elongated hypocotyl |
| d975 | = | 11 prr7–11 prr9–10 triple mutant |
| TOC1 | = | timing of CAB expression 1 |
| GI | = | GIGANTEA |
| LT50 | = | lethal temperature which 50% of the samples are dead |
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