Distinct Responses to Light in Plants

The development of almost every living organism is, to some extent, regulated by light. When discussing light regulation on biological systems, one is referring to the sun that has long been positioned in the center of the solar system. Through light regulation, all life forms have evolved around the presence of the sun. As soon our planet started to develop an atmospheric shield against most of the detrimental solar UV rays, life invaded land, and in the presence of water, it thrived. Especially for plants, light (solar radiation) is the source of energy that controls a high number of developmental aspects of growth, a process called photomorphogenesis. Once hypocotyls reach soil′s surface, its elongation deaccelerates, and the photosynthetic apparatus is established for an autotrophic growth due to the presence of light. Plants can sense light intensities, light quality, light direction, and light duration through photoreceptors that accurately detect alterations in the spectral composition (UV-B to far-red) and are located throughout the plant. The most well-known mechanism promoted by light occurring on plants is photosynthesis, which converts light energy into carbohydrates. Plants also use light to signal the beginning/end of key developmental processes such as the transition to flowering and dormancy. These two processes are particularly important for plant´s yield, since transition to flowering reduces the duration of the vegetative stage, and for plants growing under temperate or boreal climates, dormancy leads to a complete growth arrest. Understanding how light affects these processes enables plant breeders to produce crops which are able to retard the transition to flowering and avoid dormancy, increasing the yield of the plant.


Overview of Light Transduction Scheme
All life is shaped by the Earth's rotation and orbit around its own axis and the sun, providing a diurnal rhythm of day and night, and depending on the latitude, an annual cycle of day length which reaches its maximum and minimum on the solstices of summer and winter, respectively. Plants use dawn and dusk as signals to organize all aspects of their growth, such as photosynthesis. Light is an environmental factor permanently present, and yet displays a dynamic control on components of plant's functionality such as germination, phototropism, and reproduction. The decreasing number of hours of light, which starts right after the beginning of autumn, also works as an indicator to enter dormancy, preventing the detrimental effects that winter conditions might have on plant cells. Plants also react to variations of low and high light intensities (e.g., acclimation) [1], which involves a set of environmental adjustments such as leaf morphology variations, chloroplast structure, and/or modification of the composition of the photosynthetic electron transport chain, consequently affecting photosynthesis [2,3]. Plants growing under limiting light conditions show leaf and chloroplast movements toward the source of light, as well as general bending to maximize light capture, increasing photosynthetic efficiency. On the other hand, when plants are submitted to environmental conditions of high light intensity and UV-B, the chloroplasts and nucleus move away from the light, and protective photoreceptors pigments  Table 26. S proteasome pathway promoting photomorphogenesis. Pfr also induces COP1-SPA1 complex dissociation. All these pathways lead to the accumulation of major transcription factors (TFs), triggering photomorphogenesis such as HY5. (b) Two mechanisms are represented for cryptochrome signal transduction. Transcription regulation of light-activated Cry after interaction with TF CIB1 and its relatives (CIBs) leads to the activation of FT transcription, promoting floral initiation. The other mechanisms involve the interaction of cryptochromes with SPA1 proteins to suppress SPA1 activation of COP1 activity necessary for the degradation of HY5, HYH, CO, and other transcription regulators promoting photomorphogenesis. (c) ztls are activated by UV-A/blue light. Once activated, they interact with GI, resulting in the stabilization of these receptors, enabling them to act as E3 ligases which target the transcriptional regulators CDF and TOC1 for degradation. In addition, light-activated FKF1 interacts with and stabilizes CO. (d) The inactive dimeric form of UVR8 is activated to the monomeric form by UV-B, which interacts with the E3 ubiquitin ligase COP1. With the suppression of COP1, HY5 and HYH are stabilized. These two proteins, in a feed-forward loop, bind to the HY5 promoter region with further activation of transcription.
The diverse photomorphogenic responses of plants, such as seed germination, de-etiolation, and circadian clock regulation, are, to a great extent, associated with light perception by photoreceptor system [37]. Photoreceptors act through the presence of specific photoreceptive chromophores [38,39], and are the gatekeepers for different types of light sensing which are responsible for regulating a high number of physiologically and developmental downstream signaling pathways [40].

Phytochromes
It is possible to identify five photochromes in Arabidopsis: phyA, phyB, phyC, phyD, and phyE [41,42]. They are involved in several life cycle functions, including germination, de-etiolation, stomata development, flowering transition, senescence, and shade avoidance [43,44]. Phys are synthesized as a biologically inactive (Pr) form that is converted to an active (Pfr) form after red light (a) The biological active Pfr form of the phytochrome is activated by red light (R). The interaction between Pfr and PIFs triggers the rapid phosphorylation of PIFs entering protein degradation via the ubiquitin 26S proteasome pathway promoting photomorphogenesis. Pfr also induces COP1-SPA1 complex dissociation. All these pathways lead to the accumulation of major transcription factors (TFs) triggering photomorphogenesis such as HY5 (b) Two mechanisms are represented for cryptochrome signal transduction. Transcription regulation of light-activated Cry after interaction with TF CIB1 and its relatives (CIBs) leads to the activation of FT transcription, promoting floral initiation. The other mechanisms involve the interaction of cryptochromes with SPA1 proteins to suppress SPA1 activation of COP1 activity necessary for the degradation of HY5, HYH, CO, and other transcription regulators promoting photomorphogenesis. (c) ztls are activated by UV-A/blue light. Once activated, they interact with GI, resulting in the stabilization of these receptors, enabling them to act as E3 ligases which target the transcriptional regulators CDF and TOC1 for degradation. In addition, light-activated FKF1 interacts with and stabilizes CO. (d) The inactive dimeric form of UVR8 is activated to the monomeric form by UV-B, which interacts with the E3 ubiquitin ligase COP1. With the suppression of COP1, HY5 and HYH are stabilized. These two proteins, in a feed-forward loop, bind to the HY5 promoter region with further activation of transcription.

Phytochromes
It is possible to identify five photochromes in Arabidopsis: phyA, phyB, phyC, phyD, and phyE [41,42]. They are involved in several life cycle functions, including germination, de-etiolation, stomata development, flowering transition, senescence, and shade avoidance [43,44]. Phys are synthesized as a biologically inactive (Pr) form that is converted to an active (Pfr) form after red light absorption. This latter form is rapidly converted back to the inactive Pr state upon far-red light irradiation or slowly by dark reversion [45]. Pfr leads to the inhibition of several PHYTOCHROME INTERACTING FACTORs (PIFs) either by triggering their proteasome-mediated degradation or through their phosphorylation [44] (Figure 1a). The ubiquitin E3 ligase complex (COP1/SPA/FUS) is also inhibited by Pfr, enabling the stabilization of the transcription factors required for light-growth Plants 2020, 9, 894 5 of 14 development such as HY5 [46]. In the dark, upon Pfr form spontaneously change back to the Pr form after phosphorylation, it acquires the capacity to enter the nucleus and establish subnuclear foci called photobodies [47]. These are heterogeneous, meaning that they can change composition throughout the day [48,49]. Photobodies act upstream of PIFs by promoting their phosphorylation and targeting them for degradation via ubiquitination [50,51].

Cryptochromes
Arabidopsis has two cryptochromes, Cry1 and Cry2 [52], both present in the nucleus. When activated by blue light, Cry1 migrates to cytosol, while Cry2 remains in the nucleus [53]. Cry1 plays a predominant function during de-etiolation, and Cry2 displays its main role in the photoperiodic control of flowering [54]. The light-activated Cry1 binds to SPA1, leading to the inhibition of the COP1-SPA1 E3 ubiquitin ligase, which, consequently, gives rise to an accumulation of HY5 and CO transcription factors, promoting de-etiolation and flowering, respectively [55,56] ( Figure 1b). Regarding Cry2, once activated by blue light, it interacts with CRY-INTERACTING bHLH (CIB1, 2, 4, 5), directly activating the transcription factor FLOWERING LOCUS T (FT) in order to promote flowering [57]. The other CRY-interacting protein is the SUPRESSOR OF PHYTOCHROME A-105 1 (SPA1), which is responsible for positive regulation of the E3 ubiquitin ligase COP1 [55,58], leading to an inhibition of COP1 dependent degradation of transcriptional regulators such as bZIP transcription factor HYH and bHLH transcription factor HFR1 [56].

Phototropins
The photoreceptors that perceived UV-A and blue light are called phototropins (phots). Arabidopsis genome holds two: PHOT1 and PHOT2 [59]. The blue light is sensed by two flavin monoclueotide (FMN) chromophore-binding light oxygen voltage (LOV1 and LOV2) domains [60]. The conformational change promoted by light leads to autophosphorylation of the residues located both in the sensory and kinase domains [61,62]. Blue light triggers both phots but in different manners: It stimulates PHOT2 and downregulates PHOT1 [63]. These two genes are responsible for distinct mechanisms, such as phototropism and leaf positioning [64], the opening of stomas, and the accumulation of chloroplasts [65]. The activated phototropins bind to NONPHOTOTROPIC HYPOCOTYL 3 (NPH3) and ROOT PHOTOTROPISM2 (RPT2), initiating the phot signaling [66].
The mechanism of action of ZTL, LKP2, and FKF1 is through the ubiquitin-mediated degradation of clock elements such as TOC1 and PRR5 [67,69]. The interaction of FKF1, ZTL, and LKP2 with GI is induced by blue light (Figure 1c). The FKF1-GI complex interacts with CDF1 (a repressor of CO and FT expression), leading to its degradation by the ubiquitin-proteasome system with subsequent expression of CO [22] and FT. The KELCH repeats are the regions responsible for substrate proteins recognition for ubiquitination [70], and both FKF1 and LKP2 are able to interact with CDF1 [71]. In sum, the light activation of the LOV domain in the zeitlupe family members promotes an activation with GI and modification of its ubiquitin E3 ligase activity. This way, the GI-FKF1 complex actively triggers the CO repressor for degradation. With this repression lifted, CO is expressed under light, modulating flowering. The ZTL-GI complex, on the other hand, when regulated by light, limits the ZTL degradation capacity of this target proteins, controlling the circadian clock response [59].

UVR8
The UV RESISTANT LOCUS 8 (UVR8) photoreceptor is on the front line of UV-B stress-induced responses and triggers a wide range of changes in gene expression, leading to morphological adaptions and the production of flavonols that act as UV-B protective shields [72]. It also mediates phototropic bending, stomatal movement, and circadian clock cascade gene activation [73,74]. The inactive form of UVR8 is a homodimer but is converted to an active monomer after absorbing UV-B [75]. In its active monomeric form, UVR8 interacts with E3 ubiquitin ligase COP1 in the nucleus [76], leading to the expression and stabilization of HY5 and HY5 HOMOLOGUE (HYH), which, in turn, bind to the promotor of several UV-B responsive genes [77] (Figure 1d), such as those involved in the flavonoid synthesis, and chalcone synthase [78,79], which is important in abiotic and biotic stress responses. When plants are subjected to low UV-light intensities for short periods of time, their actions beneficially enhance their resistance to pathogens and herbivores [80] but increase UV-light exposure, stimulates the generation of free radicals detrimental for DNA, proteins, lipids, chloroplasts, and photosynthetic pigments, hence impairing yield [81].

Mechanisms Regulated by the Action of Light
Plants can sense light signals through photoreceptors, which are capable of transmitting those signals into a light-signaling response cascade [82]. The bHLH transcription factors PHYTOCHROME-INTERACTING FACTORs (PIFs), acting downstream of phytochromes, show a repressive action on photomorphogenesis during darkness or, in other words, promote skotomorphogenesis growth in the absence of light [44]. The PIFs family comprises PIF1/PIF3-LIKE5 (PIL5), PIF3, PIF4, PIF5/PIL6, and PIF6/PIL2 [42]. Under light conditions, active phytochromes interact with PIFs, resulting in phosphorylation and further PIFs degradation by proteasome, resulting in the photomorphogenesis responses. Recent findings on the regulation of PIF3, responsible for hypocotyl elongation, cotyledon expansion, and chloroplast development, have shown that new factors are involved in the degradation of PIF3 by the SKP1-CUL1-F-box protein complex (SCF), EIN3-BINDING F BOX PROTEINs (EBFs) 1 and 2, E3 ubiquitin LIGHT-RESPONSE BRIC-A-BRACK/TRAMTRACK/BROAD (LRB), and Photoregulatory Protein Kinases (PPKs) [83][84][85]. Regardless of PIF3's ability to bind EBFs under light or dark conditions, the recruitment of PIF3-EBFs to the SCF EBF1/2 only occurs under light and after phosphorylation of PIF3 [84]. LRB, on the other hand, only targets phyB and PIF3 under high-light environments without affecting the stability of phyB [83]. PIF3 and phyB also interact with PPKs in a light-dependent fashion, which is required for PIF3 s phosphorylation [85]. With the migration of phyB to the nucleus upon activation by light, it binds to PIF3, followed by the activation of PPK with consequent phosphorylation of PIF3. The phosphorylated PIF3 form is recognized by the LRB E3 ligases, resulting in the degradation by ubiquitination of both PIF3 and phyB [83,85].
Other PIFs are also involved in the control of germination. Specifically, PIF1 represses germination and de-etiolation [86]. This negative regulation is achieved through the action of the KELCH F-BOX protein COLD TEMPERATURE GERMINATION (CTG10), which recognizes, binds, and destabilizes PIF1, hence stimulating the completion of germination and seedling de-etiolation. This activation also shows a feedback loop where PIF1 downregulates the transcription of CTG10 [87]. Light quality also affects seed germination through the regulation of gibberelins (GA) and abscisic acid (ABA) levels. Whereas GA induces germination, ABA inhibits it. Valstij et al. [88] showed that under far-red conditions (usually shade environments), the gene MOTHER-OF-FT-AND-TFL1 (MFT) represses germination by regulating both ABA and GA signaling pathways. In the dark, PIF1 promotes the expression of ABA-INSENSITIVE 5 (ABI5), DELLA-encoding GA-INSENSITIVE (GAI), and REPRESSOR-OF-GA1 (RGA) [89]. The control of ABA and GA accumulation by PIF1 is also exerted by promoting the activation of SOMNUS (SOM), which is responsible for the increasing of ABA and decreasing of GA levels [90].

Flowering Control by CO/FT Regulation
Flowering is a fundamental phase of plant's development and is of great importance when dealing with species that are the sources of seeds which are essential for feeding purposes. Flowering regulation depends on internal and external signals such as temperature and daylength, which are converted into the regulation of two major floral integrator genes: FT and CO [91]. FT is upregulated by the protein CO in the photoperiodic pathway, which is initiated by the photoreceptors CRY1, CRY2, and FKF1 [27].
Day length must reach a threshold in order to promote the stabilization of the CO protein. Only under LD, CO is not degraded, picking its accumulation during the night [92,93]. CO, alone or combined with other factors, activates the transcription of FT gene (Figure 2). The flowering time is dependent on the amount of FT protein present in the apical meristems, which was previously transported from leaves, where the FT gene is regulated by a high number of factors. CO presents a tight transcriptional and post-transcriptional regulation, which is important to measure the day length and calculate when to promote flowering. The circadian clock FKF1, GI, and CDF are major factors in the regulation of CO [71]. In the case of CDF1 protein, it directly binds to the CO promoter and represses its expression, which results in a reduced level of CO transcripts in the morning [94] ( Figure 2a). Conversely, CDF1 is positively regulated by CCA1 and LFY at dawn and negatively regulated by PRR9, PRR7, and PRR5 in the afternoon [95].  [89]. The control of ABA and GA accumulation by PIF1 is also exerted by promoting the activation of SOMNUS (SOM), which is responsible for the increasing of ABA and decreasing of GA levels [90].

Flowering Control by CO/FT Regulation
Flowering is a fundamental phase of plant's development and is of great importance when dealing with species that are the sources of seeds which are essential for feeding purposes. Flowering regulation depends on internal and external signals such as temperature and daylength, which are converted into the regulation of two major floral integrator genes: FT and CO [91]. FT is upregulated by the protein CO in the photoperiodic pathway, which is initiated by the photoreceptors CRY1, CRY2, and FKF1 [27].
Day length must reach a threshold in order to promote the stabilization of the CO protein. Only under LD, CO is not degraded, picking its accumulation during the night [92,93]. CO, alone or combined with other factors, activates the transcription of FT gene (Figure 2). The flowering time is dependent on the amount of FT protein present in the apical meristems, which was previously transported from leaves, where the FT gene is regulated by a high number of factors. CO presents a tight transcriptional and post-transcriptional regulation, which is important to measure the day length and calculate when to promote flowering. The circadian clock FKF1, GI, and CDF are major factors in the regulation of CO [71]. In the case of CDF1 protein, it directly binds to the CO promoter and represses its expression, which results in a reduced level of CO transcripts in the morning [94] ( Figure 2a). Conversely, CDF1 is positively regulated by CCA1 and LFY at dawn and negatively regulated by PRR9, PRR7, and PRR5 in the afternoon [95]. Transcriptional regulation of FT (FT mRNA). At night, the FBHs (bHLH transcription factors) bind to the CO promoter, activating its transcription. In the morning, the presence of high amounts of CDF proteins on the CO and FT promoters repress the transcription of both genes. As afternoon is reached, FKF1 is photoactivated by blue light. At this point, it forms a complex with GI, promoting the degradation of the CDFs proteins which bind to the CO and FT promoters, freeing these promoter regions for binding to other gene activators. At the protein regulation level, the COP1-SPAs complex degrades CO protein during the night hours. When CRY1 and CRY2 are photoexcited by blue light, they acquire the capacity to interact with COP1 and SPAs, inhibiting the COP1-SPAs complex activity . At night, the FBHs (bHLH transcription factors) bind to the CO promoter, activating its transcription. In the morning, the presence of high amounts of CDF proteins on the CO and FT promoters repress the transcription of both genes. As afternoon is reached, FKF1 is photoactivated by blue light. At this point, it forms a complex with GI, promoting the degradation of the CDFs proteins which bind to the CO and FT promoters, freeing these promoter regions for binding to other gene activators. At the protein regulation level, the COP1-SPAs complex degrades CO protein during the night hours. When CRY1 and CRY2 are photoexcited by blue light, they acquire the capacity to interact with COP1 and SPAs, inhibiting the COP1-SPAs complex activity and increasing the stability of CO. PHYA also inhibits the COP1-SPAs complex. During the first hours of the day, HOS1, ubiquitin ligase, and red light activated PHYB mediate CO degradation. By the time CO picks late in the afternoon, blue light-activated FKF1 and far-red photo-activated PHYA stabilize CO. The amount of CO protein in the morning is low due to interactions with other proteins that prevents the CO-dependent activation of FT. Throughout the day, as CO becomes stable upon interaction with blue light-activated FKF1 and CRY2, activates the transcription of FT gene by directly binding to the FT promoter. The blue light-activated form of CRY2 also interacts with CIB1 and directly binds to the FT promoter, activating the transcription of the gene late in the afternoon. miR172 is a negative regulator of SMZ and SMZ protein and is a powerful repressor of FT expression under LD. TEMs transcription factors (TEM1 and TEM2) bind to FT promoter, inhibiting its transcription in the morning.
Under LD days, the FKF1-GI complex degrades CDF proteins, preventing its repression on the CO promoter [96]. As days shorten, FKF1 and GI transcription levels no longer pick at the same time. Hence, the FKF1-GI complex cannot be established, and CDF proteins are not degraded, remaining present on the CO promoter. In this way, CO transcription is prevented, which, in turn, does not activate FT expression during the day under SD [93]. Other genes are involved in the regulation of the CO-FT pathway. ZTL and LKP2 interact with FKF1 and GI to help in the destabilization of the CDF2 protein [22]. The bHLH (basic helix-loop-helix) transcription factors FLOWERING BHLH1 (FBH1), FBH2, FBH3, and FBH4 promote the activation of CO once the CDF repressor is removed from the CO promoter region [97]. Albeit CO transcripts accumulate at night both under LD and SD, their effects on the FT gene only take place at dusk under LD. CO proteins are degraded by COP1-SPA1 complex during the night (Figure 2a) [98], while during the first hours of the day, CO degradation is carried out by the HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 (HOS1), a RING finger containing E3 ubiquitin ligase [99]. PHYB also mediates CO protein degradation in the morning, contrarily to PHYA, which stabilizes CO later in the day [100]. CRY1 and CRY2 are another group of photoreceptors involved in CO protein regulation [55,101] with CRY2-SPA1 upon light activation, promoting the interaction between CRY2 and COP1 and inhibiting the capacity that COP1 has to degrade CO (Figure 2a) [55].
The transcriptional activation/inhibition of FT is the final approach for flowering regulation initiated by light sensing. The heterodimer comprising FLC and SHORT VEGETATIVE PHASE (SVP) directly suppress FT and SOC1 expression [102]. FT transcription is also inhibited by the FLC-FLM (FLOWERWING LOCUS M)-MAFs (MADS AFFECTING FLOWERING) complex [103] and by the Polycomb group complex (PRC 1-like complex) composed by the EMBRYONIC C FLOWER 1 (EMF1), LHP1 and histone E3 lysine-4 [92]. FT is negatively regulated by three more transcription factors: SCHLAFMÜTZE (SMZ), TEMPRANILLO1 (TEM1), and TEM2 (Figure 2b) [104,105]. As FT activators, one finds CIBs and CO proteins. CIBs interact directly with FT promoter, activating its expression, but the CIB1 function is restricted from late afternoon to early night and forms a complex with CRY2 after photoexcitement by blue light (Figure 2b). In the absence of blue light, CIB1 is targeted for degradation [106], while its stabilization is mediated by ZTL and LKP2 under blue light with further FT expression [101].

Conclusions
The influence of light on plant development, curiously, starts with the lack of light during seed germination until soil surface is reached. At this time, plant development suffers a transition from the heterotrophic growth, where maternally deposited energy reserves are used to fuel an autotrophic photosynthesis-dependent growth. As soon seedlings are exposed to light, fully functional chloroplasts develop, enabling photosynthesis to take place in reactions dependent on light-absorbing pigment molecules present in the thylakoids. Here, light energy is converted to chemical energy, which involves a series of chemical reactions known as the light-dependent reactions. Plants also possess five classes of photoreceptors that are differentially photoactivated based on the type of wavelengths they absorb (from far-red to UV-B). This distinguished capacity of the different photoreceptors to absorb in narrow zone of the solar spectrum allows a precise physiological response in the face of diverse signals from light, such as intensity, quality, and duration. Therefore, throughout plant's lifespan, we find mechanisms such as the circadian clock, which can be summarized as endogenous genetic pathways that allow plants to anticipate and prepare for environmental daily and seasonal changes. Among the circadian clock, we can find biological processes such as hypocotyl elongation, photosynthesis, stomatal opening, leaf movement, cell cycle progression, and flowering.
Photomorphogenesis, also defined as light-regulated plant development molecular signaling intermediates, are formed in response to the activation of photoreceptors by light. The photomorphogenic physiological responses are germination, de-etiolation, shade avoidance, Plants 2020, 9, 894 9 of 14 circadian rhythm, and flowering. Flowering was singled out in this review given its importance for plant multiplication and seed production, which is vital for animal feeding.
The present work intended to show, in a relatively brief way, that the balance between light-promoter development and growth under darkness is delicate and complex, with the capacity to influence all aspects of plant's life. If we consider the wider view of all life on Earth, having plants as the base of the food chain, it is easy to understand the importance of having a deep knowledge of how light perception is mediated by all photosynthetic organisms.