Plant Molecular Biology

, 69:409 | Cite as

Molecular interactions between light and hormone signaling to control plant growth

Article

Abstract

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.

Keywords

Gibberellins 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.

Etiolated seedlings are characterized by a highly active GA pathway, and one of its functions seems to be the repression of seedling de-etiolation in darkness (Alabadí et al. 2008). On the one hand, this is accomplished, at least, by GAs preventing accumulation of HY5, a transcription factor required for photomorphogenesis and that is a COP1-target. hy5 mutants have partially lost the ability to de-etiolate when GA biosynthesis is pharmacologically compromised. For example, hypocotyls of hy5 mutants were longer than those of the wild type when grown with paclobutrazol in darkness; this resembles the defect of hy5 mutant seedlings during de-etiolation under lights of different qualities (Koornneef et al. 1980), suggesting that the GA pathway antagonizes the positive effect of light signaling on HY5 growth-repressing activity (Alabadí et al. 2008). Then, HY5 represents an integration node between light and GA signaling pathways and the GA control on HY5 operates, at least, during etiolated growth to avoid the growth repressing effects of HY5 activity (Fig. 1).
Fig. 1

The role of hormones in the regulation of growth by light. The interactions depicted here are likely to occur very early in development, during the establishment of the seedling’s developmental program, and probably also as a mechanism to control growth later in development during day–night cycles. Seedling de-etiolation involves at least two light-dependent mechanisms: prevention of COP1 activity in the nucleus, and reduction of GA concentration by repression of GA biosynthesis genes (here represented in yellow) and induction of GA inactivation genes (not shown, for simplicity). This allows the accumulation of non-ubiquitinated HY5 and other functionally equivalent transcription factors, which are responsible for the massive transcriptional changes of light-regulated genes (represented by a CAB gene in blue). On the other hand, growth is promoted in dark periods by the circadian clock-dependent accumulation of PIF transcription factors, which are stable in the absence of light, and active in the absence of DELLA proteins, and can regulate the expression of “growth” genes through E-boxes in their promoters (here represented by EBR in green). Growth is also dependent on the regulation of brassinosteroid responsive (BRE), and auxin responsive (ARE) genes, partly through auxin-BR crosstalk. Light has been shown to modulate BR activity in certain plant species by a mechanism still unknown (in gray, see the main text), while auxin synthesis, transport and signaling is controlled, at least in adult plants, by the circadian clock (represented by the circle formed with red, blue and green arrows). Genes are shown as boxes with black arrows, and hormones are highlighted in bold

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).

Interestingly, hormones participate in the execution of different processes of SAS, including growth arrest of the newly emerging leaves, and also organ elongation. Contrary to hypocotyl or petiole elongation, which mainly occurs through cell expansion, the arrest of leaf growth during SAS is a cell-division dependent process, closely associated with a local increase in auxin signaling (and probably auxin synthesis because this arrest requires the auxin receptor TIR1) (Carabelli et al. 2007). However, the key component of this regulatory circuit are cytokinins (CKs), as indicated by the upregulation of CKX6 after exposure of young leaves to low R:FR ratios (Carabelli et al. 2007). CKX6 encodes a CK oxidase that inactivates the hormone, and is transiently upregulated also by auxin treatments (Werner et al. 2006), which suggests that the growth arrest is caused by both an auxin-dependent and a low R:FR-dependent local decrease in CK concentration in the leaves (Fig. 2).
Fig. 2

Participation of hormones in the shade-avoidance syndrome. Exposure of plants to low R:FR ratios increases the production of auxin through the TAA1-dependent biosynthetic pathway. Auxin is then responsible for the activation of CKX6 (shown in pink) in the vasculature, and the consequent reduction in CKs concentration and arrest of leaf growth associated with SAS. Detection of low R:FR ratios also triggers the rapid upregulation of expression of several genes, like bHLH and HDzip transcription factors, which interdependently regulate their downstream targets, here represented by auxin responsive (ARE) genes, E-box containing genes (EBG), and genes without E-boxes in their promoters (NEG). The stability of PIF transcription factors is also regulated by light in a PhyB-dependent manner, and their DNA-binding activity is high in this conditions thanks to the degradation of DELLA proteins under canopy-simulating low R:FR ratios. Shading also decreases blue light irradiance, which in turns allows an increase in gaseous ethylene under the canopy and promotes growth. Genes are shown as boxes with black arrows, and hormones are highlighted in bold

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.

Notes

Acknowledgments

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).

References

  1. Achard P, Vriezen WH, Van Der Straeten D, Harberd NP (2003) Ethylene regulates arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15:2816–2825PubMedCrossRefGoogle Scholar
  2. Achard P, Liao L, Jiang C, Desnos T, Bartlett J, Fu X, Harberd NP (2007) DELLAs contribute to plant photomorphogenesis. Plant Physiol 143:1163–1172PubMedCrossRefGoogle Scholar
  3. Alabadí D, Gil J, Blázquez MA, García-Martínez JL (2004) Gibberellins repress photomorphogenesis in darkness. Plant Physiol 134:1050–1057PubMedCrossRefGoogle Scholar
  4. Alabadí D, Gallego-Bartolomé J, García-Cárcel L, Orlando L, Rubio V, Martínez C, Frigerio M, Iglesias-Pedraz JM, Espinosa A, Deng XW, Blázquez MA (2008) Gibberellins modulate light signaling pathways to prevent Arabidopsis seedling de-etiolation in darkness. Plant J 53:324–335PubMedCrossRefGoogle Scholar
  5. Ballaré CL, Sánchez RA, Scopel AL, Casal JJ, Ghersa CM (1987) Early detection of neighbour plants by phytochrome perception of spectral changes in reflected sunlight. Plant Cell Environ 10:551–557Google Scholar
  6. Ballaré CL, Scopel AL, Sánchez RA (1990) Far-red radiation reflected from adjacent leaves: an early signal of competition in plant canopies. Science 247:329–332PubMedCrossRefGoogle Scholar
  7. Bancos S, Szatmari AM, Castle J, Kozma-Bognar L, Shibata K, Yokota T, Bishop GJ, Nagy F, Szekeres M (2006) Diurnal regulation of the brassinosteroid-biosynthetic CPD gene in Arabidopsis. Plant Physiol 141:299–309PubMedCrossRefGoogle Scholar
  8. Barrero JM, Rodríguez PL, Quesada V, Alabadí D, Blázquez MA, Boutin JP, Marion-Poll A, Ponce MR, Micol JL (2008) The ABA1 gene and carotenoid biosynthesis are required for late skotomorphogenic growth in Arabidopsis thaliana. Plant Cell Environ 31:227–234PubMedGoogle Scholar
  9. Bauer D, Viczian A, Kircher S, Nobis T, Nitschke R, Kunkel T, Panigrahi KC, Adam E, Fejes E, Schafer E, Nagy F (2004) Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis. Plant Cell 16:1433–1445PubMedCrossRefGoogle Scholar
  10. Carabelli M, Morelli G, Whitelam G, Ruberti I (1996) Twilight-zone and canopy shade induction of the Athb-2 homeobox gene in green plants. Proc Natl Acad Sci USA 93:3530–3535PubMedCrossRefGoogle Scholar
  11. Carabelli M, Possenti M, Sessa G, Ciolfi A, Sassi M, Morelli G, Ruberti I (2007) Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity. Genes Dev 21:1863–1868PubMedCrossRefGoogle Scholar
  12. Casal JJ, Fankhauser C, Coupland G, Blázquez MA (2004) Signalling for developmental plasticity. Trends Plant Sci 9:309–314PubMedCrossRefGoogle Scholar
  13. Castillon A, Shen H, Huq E (2007) Phytochrome interacting factors: central players in phytochrome-mediated light signaling networks. Trends Plant Sci 12:514–521PubMedCrossRefGoogle Scholar
  14. Cerdán PD, Chory J (2003) Regulation of flowering time by light quality. Nature 423:881–885PubMedCrossRefGoogle Scholar
  15. Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38:87–117PubMedCrossRefGoogle Scholar
  16. Covington MF, Harmer SL (2007) The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol 5:e222PubMedCrossRefGoogle Scholar
  17. De Grauwe L, Vandenbussche F, Tietz O, Palme K, Van Der Straeten D (2005) Auxin, ethylene and brassinosteroids: tripartite control of growth in the Arabidopsis hypocotyl. Plant Cell Physiol 46:827–836PubMedCrossRefGoogle Scholar
  18. de Lucas M, Davière JM, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484PubMedCrossRefGoogle Scholar
  19. Desgagné-Penix I, Eakanunkul S, Coles JP, Phillips AL, Hedden P, Sponsel VM (2005) The auxin transport inhibitor response 3 (tir3) allele of BIG and auxin transport inhibitors affect the gibberellin status of Arabidopsis. Plant J 41:231–242PubMedCrossRefGoogle Scholar
  20. Devlin PF, Patel SR, Whitelam GC (1998) Phytochrome E influences internode elongation and flowering time in Arabidopsis. Plant Cell 10:1479–1487PubMedCrossRefGoogle Scholar
  21. Devlin PF, Robson PR, Patel SR, Goosey L, Sharrock RA, Whitelam GC (1999) Phytochrome D acts in the shade-avoidance syndrome in Arabidopsis by controlling elongation growth and flowering time. Plant Physiol 119:909–915PubMedCrossRefGoogle Scholar
  22. Devlin PF, Yanovsky MJ, Kay SA (2003) A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiol 133:1617–1629PubMedCrossRefGoogle Scholar
  23. Djakovic-Petrovic T, de Wit M, Voesenek LA, Pierik R (2007) DELLA protein function in growth responses to canopy signals. Plant J 51:117–126PubMedCrossRefGoogle Scholar
  24. Dowson-Day MJ, Millar AJ (1999) Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant J 17:63–71PubMedCrossRefGoogle Scholar
  25. Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Chen L, Yu L, Iglesias-Pedraz JM, Kircher S, Schafer E, Fu X, Fan LM, Deng XW (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451:475–479PubMedCrossRefGoogle Scholar
  26. Fleet CM, Sun TP (2005) A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8:77–85PubMedCrossRefGoogle Scholar
  27. Franklin KA, Whitelam GC (2005) Phytochromes and shade-avoidance responses in plants. Ann Bot (Lond) 96:169–175CrossRefGoogle Scholar
  28. Gendron J, Haque A, Gendron N, Chang T, Asami T, Wang Z (2008) Chemical genetic dissection of brassinosteroid–ethylene interaction. Mol Plant 1:368–379CrossRefPubMedGoogle Scholar
  29. Gil J, García-Martínez JL (2000) Light regulation of gibberellin A1 content and expression of genes coding for GA 20-oxidase and GA 3b-hydroxylase in etiolated pea seedlings. Physiol Plant 108:223–229CrossRefGoogle Scholar
  30. Gil P, Dewey E, Friml J, Zhao Y, Snowden KC, Putterill J, Palme K, Estelle M, Chory J (2001) BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev 15:1985–1997PubMedCrossRefGoogle Scholar
  31. Halliday KJ, Fankhauser C (2003) Phytochrome-hormonal signalling networks. New Phytol 157:449–463CrossRefGoogle Scholar
  32. Hanano S, Domagalska MA, Nagy F, Davis SJ (2006) Multiple phytohormones influence distinct parameters of the plant circadian clock. Genes Cells 11:1381–1392PubMedCrossRefGoogle Scholar
  33. Hisamatsu T, King RW, Helliwell CA, Koshioka M (2005) The involvement of gibberellin 20-oxidase genes in phytochrome-regulated petiole elongation of Arabidopsis. Plant Physiol 138:1106–1116PubMedCrossRefGoogle Scholar
  34. Huq E, Quail PH (2002) PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J 21:2441–2450PubMedCrossRefGoogle Scholar
  35. Jeong DH, Lee S, Kim SL, Hwang I, An G (2007) Regulation of brassinosteroid responses by phytochrome B in rice. Plant Cell Environ 30:590–599PubMedCrossRefGoogle Scholar
  36. Jouve L, Gaspar T, Kevers C, Greppin H, Degli Agosti R (1999) Involvement of indole-3-acetic acid in the circadian growth of the first internode of Arabidopsis. Planta 209:136–142PubMedCrossRefGoogle Scholar
  37. Kanyuka K, Praekelt U, Franklin KA, Billingham OE, Hooley R, Whitelam GC, Halliday KJ (2003) Mutations in the huge Arabidopsis gene BIG affect a range of hormone and light responses. Plant J 35:57–70PubMedCrossRefGoogle Scholar
  38. Khanna R, Shen Y, Marion CM, Tsuchisaka A, Theologis A, Schafer E, Quail PH (2007) The basic helix-loop-helix transcription factor PIF5 acts on ethylene biosynthesis and phytochrome signaling by distinct mechanisms. Plant Cell 19:3915–3929PubMedCrossRefGoogle Scholar
  39. Kim J, Yi H, Choi G, Shin B, Song PS, Choi G (2003) Functional characterization of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction. Plant Cell 15:2399–2407PubMedCrossRefGoogle Scholar
  40. Knee EM, Hangarter RP, Knee M (2000) Interactions of light and ethylene in hypocotyl hook maintenance in Arabidopsis thaliana seedlings. Physiol Plant 108:208–215PubMedGoogle Scholar
  41. Knoester M, van Loon LC, van den Heuvel J, Hennig J, Bol JF, Linthorst HJ (1998) Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi. Proc Natl Acad Sci USA 95:1933–1937PubMedCrossRefGoogle Scholar
  42. Koornneef M, Rolff E, Spruit CJP (1980) Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (L.) Heynh. Z Pflanzenphysiol 100:147–160Google Scholar
  43. Lehman A, Black R, Ecker JR (1996) HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85:183–194PubMedCrossRefGoogle Scholar
  44. Li H, Johnson P, Stepanova A, Alonso JM, Ecker JR (2004) Convergence of signaling pathways in the control of differential cell growth in Arabidopsis. Dev Cell 7:193–204PubMedCrossRefGoogle Scholar
  45. Lorrain S, Allen T, Duek P, Whitelam GC, Fankhauser C (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J 53:312–323PubMedCrossRefGoogle Scholar
  46. Martínez-García JF, Santes CM, García-Martínez JL (2000) The end-of-day far-red irradiation increases gibberellin A1 content in cowpea (Vigna sinensis) epicotyls by reducing its inactivation. Physiol Plant 108:426–434Google Scholar
  47. Monte E, Tepperman JM, Al-Sady B, Kaczorowski KA, Alonso JM, Ecker JR, Li X, Zhang Y, Quail PH (2004) The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development. Proc Natl Acad Sci USA 101:16091–16098PubMedCrossRefGoogle Scholar
  48. Neff MM, Fankhauser C, Chory J (2000) Light: an indicator of time and place. Genes Dev 14:257–271PubMedGoogle Scholar
  49. Neff MM, Street IH, Turk EM, Ward JM (2005) Interaction of light and hormone signaling to mediate photomorphogenesis. In: Schafer E, Nagy F (eds) Photomorphogenesis in plants and bacteria—function and signal transduction mechanisms. Dordrecht, Springer, pp 441–445Google Scholar
  50. Nemhauser JL (2008) Dawning of a new era: photomorphogenesis as an integrated molecular network. Curr Opin Plant Biol 11:4–8PubMedCrossRefGoogle Scholar
  51. Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, Maloof JN (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448:358–361PubMedCrossRefGoogle Scholar
  52. Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof YD, Kleine-Vehn J, Morris DA, Emans N, Jurgens G, Geldner N, Friml J (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–1256PubMedCrossRefGoogle Scholar
  53. Peng J, Harberd NP (1997) Gibberellin deficiency and response mutations suppress the stem elongation phenotype of phytochrome-deficient mutants of Arabidopsis. Plant Physiol 113:1051–1058PubMedCrossRefGoogle Scholar
  54. Pierik R, Cuppens ML, Voesenek LA, Visser EJ (2004a) Interactions between ethylene and gibberellins in phytochrome-mediated shade avoidance responses in tobacco. Plant Physiol 136:2928–2936PubMedCrossRefGoogle Scholar
  55. Pierik R, Whitelam GC, Voesenek LA, de Kroon H, Visser EJ (2004b) Canopy studies on ethylene-insensitive tobacco identify ethylene as a novel element in blue light and plant–plant signalling. Plant J 38:310–319PubMedCrossRefGoogle Scholar
  56. Reed JW, Foster KR, Morgan PW, Chory J (1996) Phytochrome B affects responsiveness to gibberellins in Arabidopsis. Plant Physiol 112:337–342PubMedCrossRefGoogle Scholar
  57. Reid JB, Botwright NA, Smith JJ, O’Neill DP, Kerckhoffs LH (2002) Control of gibberellin levels and gene expression during de-etiolation in pea. Plant Physiol 128:734–741PubMedCrossRefGoogle Scholar
  58. Robson P, Whitelam GC, Smith H (1993) Selected components of the shade-avoidance syndrome are displayed in a normal manner in mutants of Arabidopsis thaliana and Brassica rapa deficient in phytochrome B. Plant Physiol 102:1179–1184PubMedGoogle Scholar
  59. Roig-Villanova I, Bou J, Sorin C, Devlin PF, Martínez-García JF (2006) Identification of primary target genes of phytochrome signaling. Early transcriptional control during shade avoidance responses in Arabidopsis. Plant Physiol 141:85–96PubMedCrossRefGoogle Scholar
  60. Roig-Villanova I, Bou-Torrent J, Galstyan A, Carretero-Paulet L, Portolés S, Rodriguez-Concepción M, Martínez-García JF (2007) Interaction of shade avoidance and auxin responses: a role for two novel atypical bHLH proteins. EMBO J 26:4756–4767PubMedCrossRefGoogle Scholar
  61. Salter MG, Franklin KA, Whitelam GC (2003) Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature 426:680–683PubMedCrossRefGoogle Scholar
  62. Savaldi-Goldstein S, Peto C, Chory J (2007) The epidermis both drives and restricts plant shoot growth. Nature 446:199–202PubMedCrossRefGoogle Scholar
  63. Sessa G, Carabelli M, Sassi M, Ciolfi A, Possenti M, Mittempergher F, Becker J, Morelli G, Ruberti I (2005) A dynamic balance between gene activation and repression regulates the shade avoidance response in Arabidopsis. Genes Dev 19:2811–2815PubMedCrossRefGoogle Scholar
  64. Shen H, Moon J, Huq E (2005) PIF1 is regulated by light-mediated degradation through the ubiquitin-26S proteasome pathway to optimize photomorphogenesis of seedlings in Arabidopsis. Plant J 44:1023–1035PubMedCrossRefGoogle Scholar
  65. Shen Y, Khanna R, Carle CM, Quail PH (2007) Phytochrome induces rapid PIF5 phosphorylation and degradation in response to red-light activation. Plant Physiol 145:1043–1051PubMedCrossRefGoogle Scholar
  66. Smalle J, Haegman M, Kurepa J, Van Montagu M, Straeten DV (1997) Ethylene can stimulate Arabidopsis hypocotyl elongation in the light. Proc Natl Acad Sci USA 94:2756–2761PubMedCrossRefGoogle Scholar
  67. Smith H (1982) Light quality, photoperception, and plant strategy. Annu Rev Plant Biol 33:481–518Google Scholar
  68. Smith H (1997) The shade-avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant Cell Environ 20:840–844CrossRefGoogle Scholar
  69. Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jurgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191PubMedCrossRefGoogle Scholar
  70. Symons GM, Reid JB (2003) Hormone levels and response during de-etiolation in pea. Planta 216:422–431PubMedGoogle Scholar
  71. Symons GM, Schultz L, Kerckhoffs LH, Davies NW, Gregory D, Reid JB (2002) Uncoupling brassinosteroid levels and de-etiolation in pea. Physiol Plant 115:311–319PubMedCrossRefGoogle Scholar
  72. Symons GM, Smith JJ, Nomura T, Davies NW, Yokota T, Reid JB (2008) The hormonal regulation of de-etiolation. Planta 227:1115–1125PubMedCrossRefGoogle Scholar
  73. Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, Cheng Y, Lim J, Zhao Y, Ballare CL, Sandberg G, Noel JP, Chory J (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176PubMedCrossRefGoogle Scholar
  74. Thain SC, Vandenbussche F, Laarhoven LJ, Dowson-Day MJ, Wang ZY, Tobin EM, Harren FJ, Millar AJ, Van Der Straeten D (2004) Circadian rhythms of ethylene emission in Arabidopsis. Plant Physiol 136:3751–3761PubMedCrossRefGoogle Scholar
  75. Turk EM, Fujioka S, Seto H, Shimada Y, Takatsuto S, Yoshida S, Denzel MA, Torres QI, Neff MM (2003) CYP72B1 inactivates brassinosteroid hormones: an intersection between photomorphogenesis and plant steroid signal transduction. Plant Physiol 133:1643–1653PubMedCrossRefGoogle Scholar
  76. Turk EM, Fujioka S, Seto H, Shimada Y, Takatsuto S, Yoshida S, Wang H, Torres QI, Ward JM, Murthy G, Zhang J, Walker JC, Neff MM (2005) BAS1 and SOB7 act redundantly to modulate Arabidopsis photomorphogenesis via unique brassinosteroid inactivation mechanisms. Plant J 42:23–34PubMedCrossRefGoogle Scholar
  77. Úbeda-Tomás S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster GT, Hedden P, Bhalerao R, Bennett MJ (2008) Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat Cell Biol 10:625–628PubMedCrossRefGoogle Scholar
  78. Vandenbussche F, Habricot Y, Condiff AS, Maldiney R, Van der Straeten D, Ahmad M (2007) HY5 is a point of convergence between cryptochrome and cytokinin signalling pathways in Arabidopsis thaliana. Plant J 49:428–441PubMedCrossRefGoogle Scholar
  79. Vriezen WH, Achard P, Harberd NP, Van Der Straeten D (2004) Ethylene-mediated enhancement of apical hook formation in etiolated Arabidopsis thaliana seedlings is gibberellin dependent. Plant J 37:505–516PubMedCrossRefGoogle Scholar
  80. Werner T, Kollmer I, Bartrina I, Holst K, Schmulling T (2006) New insights into the biology of cytokinin degradation. Plant Biol (Stuttg) 8:371–381CrossRefGoogle Scholar
  81. Yi C, Deng XW (2005) COP1—from plant photomorphogenesis to mammalian tumorigenesis. Trends Cell Biol 15:618–625PubMedCrossRefGoogle Scholar
  82. Zhao X, Yu X, Foo E, Symons GM, Lopez J, Bendehakkalu KT, Xiang J, Weller JL, Liu X, Reid JB, Lin C (2007) A study of gibberellin homeostasis and cryptochrome-mediated blue light inhibition of hypocotyl elongation. Plant Physiol 145:106–118PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Instituto de Biología Molecular y Celular de Plantas (UPV-CSIC)Universidad Politécnica de ValenciaValenciaSpain

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