Molecular interactions between light and hormone signaling to control plant growth
As sessile organisms, plants modulate their growth rate and development according to the continuous variation in the conditions of their surrounding environment, an ability referred to as plasticity. This ability relies on a web of interactions between signaling pathways triggered by endogenous and environmental cues. How changes in environmental factors are interpreted by the plant in terms of developmental or growth cues or, in other words, how they contribute to plant plasticity is a current, major question in plant biology. Light stands out among the environmental factors that shape plant development. Plants have evolved systems that allow them to monitor both quantitative and qualitative differences in the light that they perceive, that render important changes in their growth habit. In this review we focus on recent findings about how information from this environmental cue is integrated during de-etiolation and in the shade-avoidance syndrome, and modulated by several hormone pathways—the endogenous cues. In some cases the interaction between a hormone and the light signaling pathways is reciprocal, as is the case of the gibberellin pathway, whereas in other cases hormone pathways act downstream of the environmental cue to regulate growth. Moreover, the circadian clock adds an additional layer of regulation, which has been proposed to integrate the information provided by light with that provided by hormone pathways, to regulate daily growth.
KeywordsGibberellins Brassinosteroids Auxin Shade avoidance Photomorphogenesis Circadian clock Light
The growth of plant organs depends on the combination of cell division with cell expansion, which is highly regulated by environmental cues and by endogenous factors. An important component of this regulation is the temporal and spatial coordination of multiple cellular processes, so that the most adequate growth response is achieved under each particular situation—be it abiotic stress, nutritional status, developmental stage, or habitat. Support for the existence of this layer of regulation comes from the observations that growth predominantly occurs at certain times of the day (Nozue et al. 2007), and also that all the different cell types and tissues that conform a given organ respond synchronously when the appropriate growth stimulus is perceived (Savaldi-Goldstein et al. 2007; Úbeda-Tomás et al. 2008).
Light is a prevalent source of information, which can be used as a directional cue (orienting growth towards the place where more efficient photosynthesis can take place), or as an indicator of the presence of neighbours (promoting shade avoidance) (Lorrain et al. 2008). In addition, light is also critical in triggering certain transitions in development, as occurs in the switch between skoto- and photomorphogenesis, when light, for example, inhibits hypocotyl growth (Chen et al. 2004). Several plant hormones also play a regulatory role in growth responses, as learned from genetic and physiological studies (Nemhauser 2008). For instance, exogenous application of gibberellins (GAs) or brassinosteroids (BRs) increases vegetative growth, and mutants defective in the biosynthesis or signaling of these and other hormones display dwarfism and other growth-related defects.
In fact, light and hormones do not always regulate growth independently from one another. Rather, the observation that responsiveness to hormones is largely affected by light intensity or by the activity of certain photoreceptors, indicates that certain degree of interaction occurs, and it may indeed represent a mechanism to provide plasticity to growth responses (Casal et al. 2004). In this review, we will focus our attention on two of the processes in which light and hormone signaling pathways converge to regulate growth: photomorphogenesis and shade avoidance, while the differential growth in response to tropic stimuli is reviewed by XXXX in this issue. Finally, we will also describe the participation of the circadian clock in the temporal coordination of light and hormone responses.
Hormonal regulation of photomorphogenesis
Light acts as a pervasive environmental cue that affects development throughout the whole life cycle of the plant, and this is of particular significance at seedling stage (Neff et al. 2000). Upon germination, newly emerging seedlings monitor their environment and, depending on the absence or presence of light, they undergo one of two developmental programs: skoto- or photomorphogenesis, respectively. The two main characteristics of skotomophogenic growth are the promotion of hypocotyl elongation—supported by directional cell expansion—and the active maintenance of an apical hook with folded cotyledons, which can be considered as a particular form of growth because it is achieved through differential cell expansion on both sides of the hook. This program contributes to the emergence of the seedling, also minimizing deleterious effects of pushing through the soil. On the contrary, light triggers photomorphogenesis by a massive rearrangement of gene expression that includes the induction of genes encoding the machinery of photosynthesis and light protection, among other functions. Interestingly, hormones like GAs, BRs, ethylene and auxin have been attributed different roles in the regulation of this developmental switch. In this section we will discuss the evidence that supports these claims.
The genetic architecture of de-etiolation indicates that photomorphogenesis is the default pathway after germination in angiosperms, but it is repressed in darkness. The most prominent mechanism to repress photomorphogenesis in darkness is based on the COP1 system, which targets transcription factors that promote photomorphogenic development to 26S proteasome-mediated degradation (Yi and Deng 2005). Simultaneously, it allows accumulation of growth-promoting transcription factors such as PIF3 (Bauer et al. 2004). COP1, however, is not alone in this task, since several hormone pathways are actively participating in controlling this transition. For instance, ethylene, auxin, GAs, and BRs participate in both maintaining the apical hook and inducing fast hypocotyl growth, and when the proper hormonal homeostasis in dark-grown seedlings is genetically or pharmacologically disturbed both responses are affected (Achard et al. 2003; Alabadí et al. 2004; Vriezen et al. 2004; De Grauwe et al. 2005). Abscisic acid (ABA) and GAs are known to antagonize each other’s action in different stages of development, and the aba1 mutant displays defects in skotomorphogenic growth (Barrero et al. 2008). However, this phenotype does not seem to be related to the lack of ABA because a block in downstream steps of the biosynthetic pathway does not show the same phenotype, and supply of ABA does not compensate the growth defect.
One can anticipate two scenarios where interactions between the light and hormone signaling pathways to control growth may take place, those occurring before and after seedlings reach the light. In the first scenario, i.e. in etiolated seedlings, hormone pathways support this growth program by repressing photomorphogenesis, namely preventing the light signaling pathways to be active in darkness, and/or directly promoting etiolated growth, which represents another potential interaction point with light signaling. In the second scenario, i.e. during de-etiolation, light must target hormone pathways to counteract their negative effect on photomorphogenesis.
On the other hand, genetic analysis suggests that GAs regulate hypocotyl elongation in etiolated seedlings by enhancing the activity of several growth-promoting transcription factors members of the PIF family, such as PIF1, PIF3 and PIF4 (Alabadí et al. 2008). pif mutants turned out to be hypersensitive to GA deprivation, a phenotype which is similar to the one that these mutants display during de-etiolation under certain light qualities (Huq and Quail 2002; Kim et al. 2003; Monte et al. 2004; Shen et al. 2005). This phenotype denotes a likely interaction between GAs and the light signaling pathway, and the molecular basis for this interaction relies on the activity of the negative, GA signaling elements, the DELLA proteins. Under low GA concentrations, these proteins accumulate in the nucleus, while in response to GA accumulation they are degraded by the 26S proteasome pathway (Fleet and Sun 2005). Most notably, the DELLA proteins physically interact with several members of the PIF family (de Lucas et al. 2008; Feng et al. 2008), in such a way that the interaction inhibits the ability of the PIF proteins to bind to, and regulate, their target promoters. Hence, in the context of etiolated growth, the high GA status ensures low DELLA levels and therefore high PIF activity, which renders a fast-growing hypocotyl. In this case, the GA pathway reinforces the activity of PIF proteins in darkness, whose stability is regulated by light (Castillon et al. 2007). Thus, PIF proteins represent another integration node between these two signaling pathways (Fig. 1). Remarkably, the regulation of the transcriptional activity of the PIF proteins by the GA pathway, together with the regulation of their levels by light, provide a model for explaining the plastic interplay between these two pathways in the control of growth that may reach beyond the seedling stage (see below).
As stated above, other hormones have been proposed to participate in the maintenance of etiolated growth, although the molecular mechanism in these cases is far less understood than in the case of GAs, and a physiological interaction with light signaling has not been fully demonstrated. For instance, it has been shown that accurate homeostasis of ethylene is also important for the formation of the apical hook, and requires the participation of another member of the PIF family: PIF5. When this transcription factor is constitutively over-expressed, etiolated seedlings display a phenotype reminiscent of the “triple response” typical of seedlings with a hyperactive ethylene pathway: PIF5-OX seedlings have shorter hypocotyls and a more exaggerated hook than the wild type; conversely, pif5 mutants have more open hooks (Khanna et al. 2007). Importantly, the PIF5-OX etiolated seedlings have enhanced production of ethylene, most probably as a consequence of increased expression of ACS8 gene, which encodes a key enzyme on the hormone biosynthesis. It has been reported that GAs are also necessary for the formation of the apical hook (Achard et al. 2003; Alabadí et al. 2004; Vriezen et al. 2004) and, based on the interaction between DELLA and PIF proteins (de Lucas et al. 2008; Feng et al. 2008; S. Prat, personal communication), it is tempting to speculate that unfolding of the apical hook could be due to a decrease in ethylene synthesis, caused in turn, at least in part, by the accumulation of DELLA proteins upon illumination and sequestration of PIF5, although there is no experimental evidence to support this hypothesis.
The proper global hormonal homeostasis that ensures plastic growth control in etiolated seedlings is further provided by interactions between those hormone pathways with potential interaction points with light signaling, for instance the ethylene pathway, with others without obvious connections, such as the auxin or BR pathways. For example, ethylene enhances differential auxin sensitivity through the action of the ethylene-induced HOOKLESS1 protein (HLS1; Lehman et al. 1996). HLS1 encodes a putative N-acetyltransferase that has a negative effect on the levels of the AUXIN RESPONSE FACTOR2 (ARF2) protein. Since ARF2 is a negative regulator of auxin-induced differential growth, inactivation of this protein by HLS1 mediates hook maintenance by ethylene (Li et al. 2004). Auxin and ethylene may also form a regulatory loop in which auxin modulates ethylene production in the hook, then strengthening this response (De Grauwe et al. 2005). To add more complexity to this web of interactions, ethylene effects on both hypocotyl growth and hook maintenance require the activity of the growth-promoting hormone BR, most probably through the signaling branch controlled by BES1 (De Grauwe et al. 2005; Gendron et al. 2008); and, finally, BRs control auxin distribution in the apical hook (De Grauwe et al. 2005).
All of the above exemplifies how hormonal pathways important for supporting two prominent features of etiolated growth, a fast-growing hypocotyl and an apical hook, have direct or indirect potential points for cross-talk with light signaling. In natural environments, the decision to de-etiolate depends on the presence of light, and this brings us to the second scenario, in which light signaling would have to antagonize hormone action both to slow-down hypocotyl growth and to unfold the apical hook.
In agreement with the physiological role of GAs in the promotion of growth and the repression of photomorphogenesis in darkness, illumination counteracts the effect of the GA pathway by quickly decreasing the levels of bioactive GA species (Zhao et al. 2007; Symons et al. 2008), most probably as a consequence of down- and up-regulation of genes encoding key enzymes of their biosynthesis and catabolism, respectively (Achard et al. 2007; Zhao et al. 2007; Alabadí et al. 2008), with the concomitant stabilization of the DELLA proteins in, at least, a phytochrome-dependent manner (Achard et al. 2007). In fact, phyB mutants are hypersensitive to GA for hypocotyl growth under red light conditions (Reed et al. 1996). The transient deactivation of the GA pathway during de-etiolation occurs across species as it has also been described in pea and in barley (Gil and García-Martínez 2000; Reid et al. 2002; Symons et al. 2008). This rapid effect of light on hormone metabolism seems to be characteristic for GAs because it was not observed for other hormones (Symons and Reid 2003). Nonetheless, it is reasonable to think that light might also negatively impinge on ethylene biosynthesis through targeting PIF5 for degradation (Shen et al. 2007), therefore eliminating a putative positive regulator of the pathway (Khanna et al. 2007). What is clear, though, is that there is a negative effect of light on ethylene sensitivity (Knee et al. 2000), which may be related to activity of the HLS1 gene (Li et al. 2004). HLS1 protein levels are quickly reduced upon light exposure of etiolated seedlings as part of hook opening, most likely through a negative effect of light on HLS1 transcription (Li et al. 2004). Again, light antagonizes a hormone pathway as a way to trigger photomorphogenesis. A different sort of interaction occurs, however, in older, light-grown seedlings. Under certain circumstances, ethylene is able to promote hypocotyl growth (Smalle et al. 1997), a stimulatory effect that is dependent on cryptochrome-mediated blue light signaling and that needs a basal level of GA, despite of ethylene reduces GA biosynthesis at the same time (Vandenbussche et al. 2007).
In contrast with the results presented for GAs, at least two arguments downplay the possible role of BRs in the de-etiolation response. First, unlike in Arabidopsis, BR deficiency in pea does not cause a de-etiolated phenotype in darkness (Symons et al. 2002); and second, BR levels are not reduced during the exposure of Arabidopsis, pea or barley seedlings to light (Symons et al. 2008). However, the observation that far-red light increases the stability of the BR-inactivating enzyme CYP734A1 in Arabidopsis (Turk et al. 2003) opens the possibility that light acts locally to regulate BR levels in rapidly growing regions of the hypocotyl or shoot. Alternatively, it has been proposed that light would reduce BR sensitivity in Arabidopsis (Neff et al. 2005; Turk et al. 2005; Bancos et al. 2006) and rice (Jeong et al. 2007).
In the view of the available evidence, a consensus summary would be that the interaction between light and GAs is instrumental for the regulation of cell expansion in plants, while the regulatory involvement of BRs in this process has not been fully substantiated yet by experimental evidence and could be restricted to only certain species (e.g. Arabidopsis). On the other hand, the differential growth that supports the formation of the apical hook in etiolated seedlings is based on multiple interactions between GAs, ethylene and auxin, and released by light mainly through the interaction with GAs and possibly ethylene.
The participation of hormones in the shade avoidance response
Plants perceive light across a broad range of wavelengths due to the combination of multiple photoreceptors, and they use this information to detect the neighboring vegetation (Smith 1982; Ballaré et al. 1987; Ballaré et al. 1990; Smith 1997; Franklin and Whitelam 2005). In particular, direct sunlight has a high proportion of blue and red light (R), while the light reflected by neighbours, or perceived by plants growing under a dense canopy, is relatively enriched in the far-red (FR) frequencies due to absorption of red light by other plants. This shift in the spectrum of perceived light causes a change in the proportions of active and inactive phytochromes, which triggers a set of responses known as the “shade avoidance syndrome” (SAS). This response involves massive changes in gene expression (Devlin et al. 2003) and results in increased growth of certain organs like the hypocotyls, the petioles and the stem; reduction of branching; promotion of flowering (Cerdán and Chory 2003); and arrest of leaf growth (Carabelli et al. 2007). Among the photoreceptors, phyB is the major one controlling SAS (Robson et al. 1993), although other phytochromes act in conjunction with phyB to regulate specific aspects of SAS, such as phyD and phyE for petiole elongation and flowering time, and phyE for internode elongation (Devlin et al. 1998; Devlin et al. 1999).
The signaling events that regulate SAS downstream of the photoreceptors have not been completely elucidated. Several transcription factors are rapidly upregulated upon exposure to the shading effect of a dense canopy or the simulated shade of a low R:FR ratio (Devlin et al. 2003; Roig-Villanova et al. 2006). Among those, there is genetic evidence for the homeobox ATHB2/HAT4 transcription factor being a positive regulator of growth during SAS (Carabelli et al. 1996; Salter et al. 2003), while the bHLH transcription factors HFR1, PAR1 and PAR2 would act as negative regulators, possibly to prevent an exaggerated SAS (Sessa et al. 2005). HFR1 would share this role with PIL1, another bHLH protein that is necessary for full response to short-term exposure to low R:FR ratios at dawn (Salter et al. 2003), but prevents the response to prolonged low R:FR (Roig-Villanova et al. 2006). Besides, two more bHLH transcription factors, PIF4 and PIF5, have been shown to be partially responsible for elongation during SAS, and they are more stable at lower R:FR ratios (Lorrain et al. 2008).
With respect to organ elongation, other hormones seem to have more prominent roles. For instance, an increase in auxin production is essential for growth during SAS. Synthesis of auxin when SAS is triggered occurs through the activation of the metabolic pathway defined by the aminotransferase encoded by TAA1 in Arabidopsis (Tao et al. 2008). Loss-of-function mutants in TAA1 display a dramatic auxin-deficient phenotype (Stepanova et al. 2008; Tao et al. 2008), which includes the inability to promote SAS in response to low R:FR. Interestingly, although several YUCCA genes, involved in an alternative auxin biosynthetic pathway, are upregulated during SAS, they do not seem able to compensate the lack of TAA1 (Tao et al. 2008). Another indication that auxin plays a pivotal role in executing SAS is the observation that many auxin-responsive genes are misregulated in Arabidopsis transgenic plants overproducing PAR1, an atypical bHLH transcription factor which is rapidly upregulated upon exposure to low R:FR (Roig-Villanova et al. 2007). Moreover, PAR1 and its closest paralog PAR2 act as direct transcriptional repressors of several auxin-induced genes, and the phenotype of plants with reduced levels of PAR1 and PAR2 in response to low R:FR closely resembles that of hfr1, which suggests that they act as negative regulators of SAS through the interaction with auxin signaling (Fig. 2).
During development, the action of phytochromes is intimately linked to the action of GAs in the control of growth, and the interplay between phyB and GAs during SAS is a model example (Halliday and Fankhauser 2003). For instance, end-of-day FR treatments enhance GA1 levels by reducing its inactivation in the responsive stems of cowpea (Martínez-García et al. 2000). In addition, exposure of Arabidopsis to low R:FR upregulates the expression of GA biosynthesis genes (Hisamatsu et al. 2005) and GA responsiveness (Reed et al. 1996), and the elongated phenotype of phytochrome mutants is suppressed by GA deficiency and GA insensitivity (Peng and Harberd 1997). Compatible with this idea, Arabidopsis plants grown in dense cultures or under low R:FR display SAS and have lower levels of DELLA proteins, as inferred by the decrease in GFP-RGA under those conditions (Djakovic-Petrovic et al. 2007). The same decrease is observed in Arabidopsis plants grown under low intensity blue light, another cue which triggers SAS. In fact, the increase in growth promoted by low blue light does not only depend on GAs, but also on ethylene. First, ethylene production increases in dense canopies (Pierik et al. 2004a, b). Second, ethylene application at concentrations found in dense canopies promotes SAS in isolated tobacco plants (Pierik et al. 2004a, b). Third, transgenic tobacco plants that are insensitive to ethylene are impaired in triggering SAS (Knoester et al. 1998). And fourth, all traits associated with SAS in tobacco are triggered by low blue light, and are impaired in ethylene insensitive plants. However, while the response of ethylene to low intensity blue light seems to be independent of GAs, low R:FR ratios also increase the production of ethylene in a GA-dependent fashion (Pierik et al. 2004a, b).
In summary, the robustness observed in a complex physiological response like SAS seems to rely on the high degree of connectivity between signaling pathways, including those involved in light-quality perception, and also hormone signaling pathways (Fig. 2). Part of this complexity is also revealed by mutations such as those in BIG/TIR3, which provoke pleiotropic defects in SAS and in several other hormone-regulated processes, probably due to a primary defect in auxin transport (Gil et al. 2001; Kanyuka et al. 2003; Desgagné-Penix et al. 2005; Paciorek et al. 2005).
Temporal coordination of growth: hormones under clock control
As described in the previous sections, interactions between light and hormone signaling pathways are particularly evident—but not only—during de-etiolation and under a canopy. These are special situations that occur just once in the life of a plant, in the case of de-etiolation, or that may never occur, in the case that plants live in communities at very low density and never experience neighbors’ shade. Growth, however, occurs on a daily basis reaching maximum rates during the second half of the night (Jouve et al. 1999; Nozue et al. 2007). The daily control is due to a concerted action of both light signaling, which represses growth during the day, and the circadian clock that gates growth towards the end of the night (Nozue et al. 2007). This element draws a new scenario with new questions; for example, does light repress growth during the day by canceling the growth promoting effect of hormone pathways? Does the circadian clock gate hormone signaling as part of its control over growth rate? The reasonable answer to these questions is yes, though supporting experimental evidence is scarce (Fig. 1).
In the model proposed by Nozue et al. (2007) to explain rhythmic growth, the transcription factors PIF4 and PIF5 are key elements: during the day, light inactivates these PIF factors by promoting their 26S proteasome-mediated degradation, whereas early in the night the circadian clock does not allow their transcription. This leaves a narrow window of a few hours before dawn to grow. Besides, PIF activity is guaranteed in that period of time, given a reduction in the levels of DELLA proteins (Achard et al. 2007). In those conditions, the inhibitory interaction between DELLA and PIF proteins (de Lucas et al. 2008; Feng et al. 2008) is disfavored. Conversely, light-dependent accumulation of DELLA proteins during the day (Achard et al. 2007) may inhibit the activity of basal levels of PIF proteins, thus reinforcing the restraining effect of light. Therefore, it seems that the primary effect of the GA pathway in the daily control of growth would be to control post-translational regulation of PIF proteins, since GAs seem to have a minor role—if any—in modulating PIF4 and PIF5 daily transcription through an interference with the activity of the circadian clock (Hanano et al. 2006). Nonetheless, circadian regulation of transcript levels of several genes coding for GA-metabolism enzymes has been described (Zhao et al. 2007). For instance, expression of two genes encoding GA catabolic enzymes, AtGA2ox1 and AtGA2ox2, shows maximum levels during light periods, which may be important for maintaining low GA levels at phases of the day when growth has to be restrained.
Other hormone pathways, such as those of ethylene and BR, are also under clock control (Thain et al. 2004; Bancos et al. 2006). However, no direct effects on the rhythmic hypocotyl growth have been reported for any of the two pathways. In fact, ethylene and BR levels oscillate out of phase with respect to the rhythm of hypocotyl growth, and mutants deficient in ethylene signaling do not affect rhythmic growth at all (Thain et al. 2004; Bancos et al. 2006). The circadian clock exerts, however, a very strong influence on the transcriptional activity of genes of the auxin pathway, with an impact on hypocotyl and stem growth (Covington and Harmer 2007). This control is also visible in the circadian oscillation of IAA levels in Arabidopsis inflorescence stems (Jouve et al. 1999). Transcriptional regulation of auxin activity by the circadian clock is achieved at multiple levels: it affects auxin biosynthesis, transport, perception, and signaling, and it therefore determines the temporal expression of many downstream auxin-regulated genes. More importantly, the overall consequence of this regulation is that the circadian clock gates the ability of auxin to induce hypocotyl growth. Under constant light, the phase of maximum growth of seedlings entrained in day–night cycles occurs at subjective dusk (Dowson-Day and Millar 1999), and maximum auxin sensitivity is set by the clock at that time of the day (Covington and Harmer 2007). A prediction of the model that emerges based on these data is that the phase of maximum auxin-induced growth can be shifted towards the end of the night under entraining conditions, for example under short-day photoperiod (Nozue et al. 2007).
In summary, with the physiological and molecular evidence available at this point, it seems reasonable to propose that both the plasticity and the robustness of growth responses in plants are based on the framework provided by multiple interactions between light and hormone action, reinforced by the additional layer of regulation that represents the connections between hormones and the circadian clock. Still, many fundamental issues need to be addressed. In particular, it is becoming apparent that interactions between hormones, or between hormones and other signaling cues, operate through distinct molecular mechanisms and have a variable output depending on the cell type and the developmental stage. But we still lack the approriate tools, for instance, to analyze variation of hormone concentration at the cell-scale resolution, and to model the interactions between multiple elements expressed in different cell types. And, finally, an additional effort should also be devoted to study how signaling networks evolve, and to understand the adaptive value of the interactions described.
We thank Verónica Arana, Juan Carbonell and Jaime Martínez-García for discussions and comments on the manuscript, and we apologize for not including all of our colleagues’ extensive contributions to the field, due to space constrains. Work in the authors’ laboratory is funded by the Spanish Ministry of Science (BIO2007-60923).
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