Year: 2011
Type: article
Abstract: Plant development and growth are extremely plastic in response to changes in ambient light conditions. Light is not only the ultimate energy source for photosynthesis; its physical parameters, such as quality, intensity, direction, and duration, also serve as key environmental and time cues (Chen et al., 2004). Therefore, it is vital for plants to closely monitor and precisely respond to changes in light properties in order to optimize growth under a wide range of ecological environments and to synchronize developmental transitions with diurnal and seasonal time. Plants have evolved to “see” the light spectrum between 280 and 750 nm, which spans UV-B, UV-A, and visible light, through five classes of photoreceptors. In the reference plant Arabidopsis (Arabidopsis thaliana), they include the newly determined UV-B receptor UV RESISTANCE LOCUS8 (UVR8; Kaiserli and Jenkins, 2007; Rizzini et al., 2011); three types of UV-A/blue light receptors, including cryptochromes (cry1 to 3; Kleine et al., 2003; Yu et al., 2010; Chaves et al., 2011), phototropins (phot1 and 2; Briggs and Christie, 2002), and the family of ZEITLUPE/FLAVIN-BINDING, KELCH, F-BOX1 (FKF1)/LOV KELCH PROTEIN2 (LKP2; Nelson et al., 2000; Somers et al., 2000; Schultz et al., 2001); and the red and far-red sensing phytochromes (phyA to E; Quail, 2010). Collectively, these photoreceptors regulate almost every facet of plant development and growth from seed germination to floral initiation (Franklin and Quail, 2010; Kami et al., 2010). Many light responses are mediated by alterations in gene expression. Among the 15 photoreceptors discovered so far, 10 of them, UVR8 (Kaiserli and Jenkins, 2007; Favory et al., 2009), cry1 (Wu and Spalding, 2007), cry2 (Kleiner et al., 1999; Yu et al., 2009), FKF1 (Sawa et al., 2007; Fornara et al., 2009), LKP2 (Yasuhara et al., 2004), and phyA to E (Sakamoto and Nagatani, 1996; Yamaguchi et al., 1999; Kircher et al., 2002), have been shown to localize to the nucleus, where they regulate gene expression in a light-dependent manner (Jiao et al., 2007). An emerging common mechanism for such light-dependent gene expression is through regulating the stability of key transcriptional regulators (discussed below; Yi and Deng, 2005; Brown et al., 2009; Chen and Chory, 2011; Leivar and Quail, 2011). At the cellular level, photoactivation of photoreceptors triggers the rapid localization of a number of them, including phyA to E, cry2, and possibly cry1 and UVR8, to discrete subnuclear foci or nuclear bodies (Kleiner et al., 1999; Yamaguchi et al., 1999; Wang et al., 2001; Kircher et al., 2002; Favory et al., 2009; Yu et al., 2009; Gu et al., 2011; Lian et al., 2011; Liu et al., 2011). Nuclear bodies are morphologically distinct subnuclear domains that provide microenvironments for the regulation of protein dynamics, gene expression, and DNA replication and repair in both plant and animal cells (Shaw and Brown, 2004; Spector, 2006). The general principles of nuclear body function and assembly are still largely unknown. The photoreceptor-containing nuclear bodies, or “photobodies,” found in plants are a unique type of subnuclear domain whose size, number, and potentially function are directly regulated by external light cues (Chen and Chory, 2011). Observations of these speckle-shaped photobodies have raised many questions. How is the formation of photobodies regulated? What are the functions of the photobodies? What are the factors required for photobody formation? These are some of the key questions that are being actively investigated. Further understanding of photobody function and regulation will not only be important for understanding the subcellular organization of light signaling events in plants but also could potentially uncover general principles governing subnuclear domains in higher eukaryotes. In this review, we will summarize recent developments related to phy-containing photobodies, touch briefly on photobodies containing crys, and discuss the potential functions of photobodies in relationship to protein degradation and gene expression. For more comprehensive coverage of light signaling in plants, the reader is referred to the following recent reviews (Henriques et al., 2009; Jenkins, 2009; Chory, 2010; Franklin and Quail, 2010; Kami et al., 2010; Lau and Deng, 2010; Möglich et al., 2010; Nagatani, 2010; Rockwell and Lagarias, 2010; Yu et al., 2010; Chaves et al., 2011; Chen and Chory, 2011; Leivar and Quail, 2011; Ulijasz and Vierstra, 2011). Phys in higher plants are red (R) and far-red (FR) light receptors that use a linear tetrapyrrole, phytochromobilin, as their chromophore. Phys can interconvert between two relatively stable conformers: an R light-absorbing inactive Pr form (λmax = 660) and a FR light-absorbing active Pfr form (λmax = 730; Rockwell et al., 2006). Although it was initially thought that phys localized and functioned primarily in the cytoplasm, a series of studies performed over a decade ago using GUS-tagged and fluorescent protein-tagged phys convincingly demonstrated that photoactivation from the Pr to the Pfr form results in the rapid translocation of phys from the cytoplasm to the nucleus (Sakamoto and Nagatani, 1996; Kircher et al., 1999, 2002; Yamaguchi et al., 1999; Kim et al., 2000). This change in localization is one of the earliest phy responses to light; for both phyA and phyB, the most prominent phys in Arabidopsis, nuclear accumulation is required for most of their downstream responses (Huq et al., 2003; Genoud et al., 2008). It was first reported by Akira Nagatani and colleagues that photoactivated phyB-GFP was not only localized to the nucleus but also further compartmentalized to subnuclear speckle-like photobodies (Yamaguchi et al., 1999). Parallel studies by Eberhard Schäfer, Ferenc Nagy, and colleagues demonstrated that all five Arabidopsis phys, phyA to E, localize to photobodies in the light and that phy photobody localization is conserved in both dicotyledonous and monocotyledonous plants (Kircher et al., 1999, 2002; Kim et al., 2000). Although most studies on phy photobodies were conducted using transgenic lines that overexpressed fluorescent protein-tagged phys, both native pea (Pisum sativum) phyA and Arabidopsis phyB photobodies have been observed using immunocytochemistry, suggesting that the formation of photobodies is not an artifact of phy overexpression (Hisada et al., 2000; Kircher et al., 2002). The translocation of phys to photobodies happens very quickly during the dark-to-light transition; photobodies containing both phyA and phyB can be observed after 1 to 2 min of R light exposure (Bauer et al., 2004). PhyB photobody localization is triggered by R light (Yamaguchi et al., 1999; Kircher et al., 2002). In contrast, phyA photobody localization is triggered by R, FR, and blue light (Kim et al., 2000). These “early” photobodies are transient and disappear after 1 h of light exposure (Bauer et al., 2004). Phy photobodies reappear after 2 h in R light and remain present in the light (Yamaguchi et al., 1999; Bauer et al., 2004). These “late” photobodies contain mainly phyB, because phyA is rapidly degraded in R light (Kim et al., 2000; Kircher et al., 2002). Joanne Chory and colleagues showed that the steady-state pattern (size and number) of phyB photobodies under continuous R light is determined by the percentage of phyB in the Pfr form at a given moment (Chen et al., 2003). Light conditions that shift the Pr/Pfr equilibrium to the Pfr side or stabilize the Pfr form will promote large phy photobody formation. Consistent with this notion, under high-intensity R light, which drives the equilibrium to the Pfr form, phyB appears to be localized exclusively to a few large photobodies with diameters between 1 and 2 μm (Chen et al., 2003, 2010b). By contrast, under dim R light or light with a low R-to-FR ratio, where more phyB stays in the Pr form, phyB tends to localize to many smaller photobodies or localizes diffusely in the nucleoplasm (Fig. 1; Chen et al., 2003). The formation of large phyB photobodies correlates tightly with the light-dependent hypocotyl inhibition response. The fact that the steady-state pattern of phyB-GFP is predictable and can be precisely manipulated by external light quantity and quality makes it an excellent visible readout for genetic screens (discussed below; Chen, 2008). Although phyB photobodies appear to be morphologically stable, they are actually quite dynamic subnuclear domains; fluorescence recovery after photobleaching experiments on phyB-yellow fluorescent protein (YFP) photobodies showed that photobody-associated phyB-YFP is rapidly exchanged with nucleoplasmic phyB-YFP (Rausenberger et al., 2010). The morphology of phy photobodies is directly regulated by light. Confocal images of phyB-GFP localization patterns and corresponding PBG seedlings under increasing intensities of red light are shown. PhyB-GFP is evenly distributed under dim (0.5 μmol m−2 s−1) R light. With increasing R light intensity (1 μmol m−2 s−1 and 2 μmol m−2 s−1), phyB-GFP starts to form exclusively small, or both small and large photobodies, respectively. Under strong R light (above 8 μmol m−2 s−1), phyB-GFP localizes exclusively to large photobodies. The localization of phyB-GFP correlates with the degree of hypocotyl inhibition in the light. Some phy photobodies might also contain the blue light receptor cry2. Crys are photolyase-like photoreceptors that use FAD as the chromophore. When phyB-GFP and cry2-red fluorescent protein were coexpressed in BY-2 protoplasts, not only did they colocalize on photobodies, they could also be coimmunoprecipitated (Más et al., 2000). Because cry2 is photolabile and rapidly degraded in blue light, it could be colocalized with phyB in early photobodies during the dark-to-light transition. Consistent with this hypothesis, cry2 photobody localization is also a rapid light response, as Arabidopsis cry2 is translocated to photobodies within 15 min after blue light exposure (Yu et al., 2009). Activated cry1 has also been suggested to localize to nuclear bodies (Wang et al., 2001; Gu et al., 2011; Lian et al., 2011; Liu et al., 2011). Because cry1 and cry2 were colocalized with COP1 and SPA1 on nuclear bodies (Gu et al., 2011; Lian et al., 2011; Liu et al., 2011; Zuo et al., 2011), it is likely that cry1, similar to cry2, could also localize to phy-containing photobodies in the light. The intramolecular requirements for photobody localization have been most extensively studied using Arabidopsis phyB. Two general approaches have been taken to dissect the phy subdomains required for photobody localization: one approach is to examine the localization pattern of phy truncation fragments; the other approach is to characterize the localization pattern of loss-of-function or gain-of-function alleles of phy. The domain structure of phys has been well defined. Phys can form either homodimers or heterodimers (Clack et al., 2009); each monomer is an approximately 125-kD polypeptide. The phy protein can be divided into two domains: an N-terminal photosensory and signaling domain and a C-terminal dimerization domain, with a hinge region connecting the two (Fig. 2; Nagatani, 2010). The N-terminal domain comprises four subdomains: an N-terminal extension (NTE); a PAS (for PER, ARNT, and SIM) domain; a GAF (for cGMP phosphodiesterase, adenylate cyclase, and FhlA) domain, which contains a conserved Cys residue forming a thioether linkage with the A ring of the chromophore phytochromobilin; and a PHY (for phytochrome-specific GAF-related) domain (Rockwell et al., 2006). The crystal structure of the PAS/GAF domain of the bacteriophytochrome DrBph1 from Deinococcus radiodurans revealed the presence of a light-sensing knot, which plays an important role in signaling. For example, amino acid residues located in the knot are involved in the interaction with phytochrome-interacting factors (PIFs; Oka et al., 2008; Kikis et al., 2009; Nagatani, 2010; Ulijasz and Vierstra, 2011). The C-terminal half of phys contains two subdomains, a PAS-related domain (PRD) containing two PAS domains (PAS-A and PAS-B) and a His kinase-related domain (HKRD; Rockwell et al., 2006). Structural basis for phyB localization and signaling. Phys can be divided into the N-terminal light-sensing and signaling domain and the C-terminal dimerization and localization domain (Nagatani, 2010). The GAF and PHY domains of phyB physically interact with the PRD to mask nuclear localization signals located in the PRD (Chen et al., 2005). Additionally, although the PRD alone is sufficient for nuclear import, the PRD and HKRD together are required for normal phyB photobody localization (Matsushita et al., 2003; Chen et al., 2005). Mutations in red are those that have apparently normal photobody localization but fail to complement a null phyB mutant, possibly due to reduced interaction with PIF proteins (Oka et al., 2008; Kikis et al., 2009). The Y276H mutation, in green, causes constitutive phyB localization to large photobodies and constitutive phytochrome signaling (Su and Lagarias, 2007). The G767R mutation, in brown, results in the inability of phyB to localize to the nucleus (Matsushita et al., 2003). All other mutations, represented in blue, show abnormal photobody localization as well as impaired light signaling (Kircher et al., 2002; Chen et al., 2003; Oka et al., 2008). Specifically, mutant G118R does not incorporate the chromophore; mutants C327Y and A587T show slightly faster dark and mutant a slightly spectrum in to dark The chromophore is represented by four studies have revealed that the C-terminal half of phyB localizes to photobodies of light (Chen et al., 2003; et al., 2003). the photobody localization of phyA also its C-terminal half et al., 2011). the C-terminal domain of phyB, the PRD is both required and sufficient for nuclear suggesting that it either a nuclear localization or is to to an protein containing a (Matsushita et al., 2003; Chen et al., 2005). the PRD and HKRD are required for normal photobody localization (Chen et al., 2005). Consistent with this notion, that in nuclear or photobody localization have been within the PRD (Fig. 2; Kircher et al., 2002; Chen et al., 2003; et al., 2003). The role of the HKRD in photobody localization is still a although the HKRD not localize to photobodies, a phyB truncation a of the HKRD could still form smaller photobodies (Chen et al., 2005). Because nuclear and photobody localization are both light it the of the N-terminal photosensory domain the C-terminal localization The is in the Pr form, C-terminal localization signals are by the N-terminal domain through an interaction between the subdomains and the both the and photobody localization signals are in the Pfr form as a of light-dependent changes 2008; and Chen, 2008). The of the Pfr form could also domains required for with other signaling Consistent with the that the of Pfr is important for photobody the which plays a role in the Pfr form, is also required for phyB photobody formation (Chen et al., 2005). studies of phyB alleles have further demonstrated that the Pfr form of phyB is required for photobody N-terminal loss-of-function phyB alleles that are in photobody localization also have stable and some have abnormal light (Fig. 2; Chen et al., 2003; Oka et al., 2008). By contrast, a active phyB mutant, localizes to photobodies of light conditions (Su and Lagarias, 2007). loss-of-function that only signaling but not the properties of phyB have normal photobody localization patterns (Oka et al., 2008; Kikis et al., 2009), which further that the photobody localization on phyB being in the Pfr form and is not a of phy signaling. the of phy photobodies, has been their is that the photobodies are for active photoreceptors but are not required for light signaling (Fig. In this photobodies serve as a to regulate the of active phy in the Consistent with this the of phyB to a dimerization domain and a is active in light responses but does not localize to photobodies (Matsushita et al., 2003; et al., 2010). from localization and studies on light signaling the that photobodies might be the of light signaling. of photobody The In this the of photoactivated nucleoplasmic phys is regulated by within photobodies. These photobodies serve as that the phys into the nucleoplasm to their signaling in the regulation of The degradation In this the photobodies are for the and degradation of key transcriptional The regulators localize to photobodies, their DNA with The expression of the is regulated within or in the of the photobodies. transcriptional responses of the et al., et al., 2007; et al., 2009; Leivar et al., 2009; et al., 2009). Two emerging signaling that the key signaling events regulating gene expression by the stability of either or The factors include the (for hypocotyl et al., et al., the (for after far-red light 1; et al., the (for hypocotyl in far-red 1; et al., and some of the family et al., 2008; et al., 2009), including et al., Liu et al., (for et al., (for protein (for et al., 2011; et al., and et al., 2007). These proteins are degraded in the dark by the COP1 (for the (for protein (for of phytochrome where COP1 and of the family of proteins form the et al., 2000; et al., 2003; et al., 2004; et al., 2005; et al., 2005; et al., 2007; et al., Liu et al., 2008; Chen et al., et al., 2011). COP1 is also involved in the of both phyA and phyB, as a mechanism to phy signaling in the light et al., 2004; et al., 2010). The is that phys promote the stability of this of regulators by (Chen and Chory, 2011). Although the mechanism of phys COP1 the COP1 is still it has been shown that directly regulate either the formation of the receptor or the interaction between the receptor and its proteins et al., 2011; Liu et al., 2011; Zuo et al., 2011). It is quite that phys could a similar mechanism to regulate the of transcriptional are also transcriptional regulators that are to phy signaling. Some of the of this are the et al., et al., 2007; et al., 2008; et al., 2009; et al., 2009; Leivar and Quail, 2011). Phys directly to and their and degradation in the light et al., Leivar and Quail, 2011). The rapid of in the light is a key mechanism to on responses et al., 2009; et al., 2009). is that photobodies are for protein degradation (Fig. This is by the fact that many signaling are localized to photobodies to their degradation For example, during the dark-to-light in both phyA and colocalize to early phy photobodies their degradation et al., 2006). In the transcriptional including and some also colocalize with COP1 on nuclear bodies of the protein family have also been colocalized with COP1 on nuclear bodies et al., 2003; et al., 2008). These results that these transcriptional regulators could at be on photobodies. In photobodies be with cry2 degradation (Yu et al., 2009). A of light signaling that have been shown to localize to photobodies or subnuclear These include not only photoreceptors but a number of transcriptional regulators and their suggesting that photobodies are involved in protein degradation A of light signaling that have been shown to localize to photobodies or subnuclear These include not only photoreceptors but a number of transcriptional regulators and their suggesting that photobodies are involved in protein degradation In of the have been shown to localize to subnuclear foci et al., 2002). it has not been demonstrated the with photobodies in In the Arabidopsis and were shown to localize to the nucleoplasm et al., 1999). and the other two key of the also localize to the nucleoplasm et al., 2008). In which is the key of the that the of localizes to the nucleoplasm in both and Arabidopsis and hypocotyl et al., 1996; et al., these results the that the protein are on photobodies and are degraded in the into the of photobodies will further this Although photobodies are likely involved in protein it is quite that not all of their are to protein For example, is localized to phy photobodies but is stable in the light et al., 2008). What other functions could photobodies have protein is that photobodies are involved in transcriptional regulation (Fig. This is by the fact that many of the photobody are transcriptional which could their to the of photobodies. The between nuclear bodies and transcriptional regulation is well et al., 2009). For example, protein bodies have been shown to the higher order of the and they regulate the expression of in lines by between and et al., 2007). phy photobodies could serve as organization involved in the regulation of (Fig. This and the degradation in are not as the degradation of some transcriptional has been shown to be with their transcriptional et al., 2005; and 2006). Therefore, it is also that photobodies are for both the degradation of transcriptional regulators and the regulation of Although nuclear bodies have been extensively in and key of a few nuclear bodies have been by and approaches 2000; and 2007), the function and regulation of nuclear bodies are still Arabidopsis an to dissect the function of nuclear bodies by the of genetic and approaches (Shaw and Brown, 2004; et al., and Spector, 2010). Because their steady-state pattern can be precisely manipulated by external light quality and photobodies provide an excellent to the function and of nuclear bodies in to signaling events in the nucleus 2008). reported a genetic at mutants in phyB-GFP photobody localization in the light (Chen et al., 2010b). This a phy signaling which is localized to the of phyB photobodies. The mutant a of light signaling mutants that are and in R and FR light. In phyB-GFP localizes to smaller photobodies in (Fig. in and in the light (Chen et al., 2010b). is to be similar to which is a receptor that proteins to the for suggesting that could a similar role in and degradation in the light (Chen et al., 2010b). these results provide genetic the in which photobodies are for protein degradation (Fig. Chen et al., 2010b). Further of the functions of as well as the of other from the genetic will likely provide into the between photobodies and protein The of PBG type of and mutant seedlings under 8 μmol m−2 s−1 light. The has both and Confocal images show that phyB-GFP is localized to large photobodies in PBG By contrast, phyB-GFP to form large photobodies and is localized to smaller photobodies in photobodies in plants are unique and subnuclear domains whose assembly and function are directly regulated by light. The localization of including phys and crys, to photobodies is triggered by a to their active It is likely that the exposure of domains in the active such as the C-terminal domain of phyB, and the or of photoreceptors and other signaling to photobodies. The mechanism of photobody assembly is still studies of light signaling and recent genetic the that photobodies are for light signaling such as light-dependent of key transcriptional we have only to the and functions of photobodies. Many key questions remain to be It is still not transcriptional regulators are degraded or only on photobodies. still not photobodies are directly involved in transcriptional regulation and they are with a between the light signaling and other signaling including those of and the on downstream signaling et al., 2010; Lau and Deng, 2010; Leivar and Quail, 2011). photobodies serve as a for the interaction between these signaling that by using a of and studies over the few to some of these questions and uncover of function and for photobodies in light signaling.
Source: PLANT PHYSIOLOGY
Institution: Duke University
Language: English
Topic: Light effects on plants
Subfield: Plant Science
Domain: Life Sciences
Open Access status: bronze
Awards: G7123896175, G8934754145
OpenAlex ID: W1986240684