Identification of photoperception and light signal transduction pathways in citrus

DEVELOPMENTAL PROCESSES

RESEARCH ARTICLE

Identification of photoperception and light signal transduction pathways in citrus

Vera Quecini

Instituto Agronômico de Campinas, Centro de Pesquisa e Desenvolvimento de Recursos Genéticos, Campinas, SP, Brazil

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ABSTRACT

Studies employing model species have elucidated several aspects of photoperception and light signal transduction that control plant development. However, the information available for economically important crops is scarce. Citrus genome databases of expressed sequence tags (EST) were investigated in order to identify genes coding for functionally characterized proteins responsible for light-regulated developmental control in model plants. Approximately 176,200 EST sequences from 53 libraries were queried and all bona fide and putative photoreceptor gene families were found in citrus species. We have identified 53 orthologs for several families of transcriptional regulators and cytoplasmic proteins mediating photoreceptor-induced responses although some important Arabidopsis phytochrome- and cryptochrome-signaling components are absent from citrus sequence databases. The main gene families responsible for phototropin-mediated signal transduction were present in citrus transcriptome, including general regulatory factors (14-3-3 proteins), scaffolding elements and auxin-responsive transcription factors and transporters. A working model of light perception, signal transduction and response-eliciting in citrus is proposed based on the identified key components. These results demonstrate the power of comparative genomics between model systems and economically important crop species to elucidate several aspects of plant physiology and metabolism.

Key words: cryptochrome, data mining, light signaling, phototropin, phytochrome.

Introduction

Plant development is highly plastic, allowing the environment to exert tight control over the transitions between genetic developmental programs in order to maximize growth and reproduction (Meyerowitz, 2002). Light provides spatial and temporal information to regulate plant development throughout its life cycle: from germination and seedling establishment to the onset of the reproductive stage (Schäfer and Nagy, 2006). Plants are able to detect environmental light direction, duration, fluency and wavelength due to a complex system of photoreceptor molecules: the blue (B) and ultraviolet-A (UV-A) 320-500 nm light-sensing cryptochromes (cry) and phototropins (phot) (Banerjee and Batschauer, 2005) and the red (R)/far red (FR) 600-750 nm phytochrome (phy) receptors (Schepens et al., 2004). Recently, a novel family of putative B photoreceptors has been described in Arabidopsis thaliana: the ZEITLUPE (ZTL)/ Flavin-binding Kelch repeat F-box protein (FKF1)/LOV Kelch Protein (LKP2) family (Nelson et al., 2000; Schultz et al., 2001; Somers et al., 2000). ZTL/ FKF1/LKP2 are involved in the circadian clock mechanism and photoperiodic flowering response (Imaizumi et al., 2005).

In higher plants, photoreceptor co-action is a common theme and the pathways may function synergistically, antagonistically and additively to control several developmental responses (Schäfer and Nagy, 2006). Moreover, plant photoreceptors operate in concert with numerous other signaling systems; including phytohormones, carbohydrate-mediated, temperature, gravity and the endogenous clock transduction pathways (Halliday and Fankhauser, 2003; Chen et al., 2004; Heggie and Halliday, 2005). The molecular mechanisms involved in light-induced signal transduction include the following: light-regulated sub-cellular localization of the photoreceptors (Guo et al., 1999; Nagy and Schäfer, 2002; Chen et al., 2005; Kong et al., 2006); a large reorganization of the transcriptional program (Casal and Yanovsky, 2005; Franklin et al., 2005) and light-regulated proteolytic degradation of several photoreceptors and signaling components (Höcker, 2005; Huq, 2006).

Studies employing model plant species have demonstrated that photoperception, the signal transduction pathways and the responses elicited by light form a complex interconnected network rather than a linear pathway (Chen et al., 2004; Quecini and Liscum, 2006). The diversity of light responsiveness observed in plants has arisen from the elaboration, combination and re-arrangement of a basic repertoire of mechanisms responsible for light-mediated developmental regulation, allowing adaptation to a wide range of climatic and latitudinal regions. Comparative genomics has provided tools to access the genetic bases of this diversity in non-model species using bioinformatics, which increases the fundamental knowledge of gene interactions and permits analyses of the functional significance of proteins in silico (e.g. Santelli and Siviero, 2001; Souza et al., 2001; Hecht et al., 2005).

Virtually all information about light-regulated development in woody plants comes from studies with Populus, a temperate deciduous perennial (Zhu and Coleman, 2001; Olsen and Juntilla, 2002). Adaptive traits in temperate perennial woody plants involve an integrated physiological response directed at plant survival and nutrient storage over the winter period and are greatly dependent of photoreceptor-mediated perception of seasonal progression (Thomas and Vince-Prue, 1997). Surprisingly, recent evidence has demonstrated that light is also the main factor triggering the transition between vegetative to reproductive developmental stages of trees in Equatorial regions (Borchert et al., 2005). The effects of light on developmental processes in citrus and other neotropical tree species have been described in several situations, although without approaching the molecular aspects of the metabolism (Steppe et al., 2006; Chen L-S et al., 2005; Raveh et al., 2003; Torné et al., 2001). Mutant studies employing transgenically generated plants have demonstrated variable extents of functional conservation in the genes responsible for developmental control between citrus and model species (Pena et al., 2001; Pillitteri et al., 2004). However, the detailed functional characterization of individual genes is a limiting factor in the study of tree species, and new strategies should be devised for the study of gene function (Groover and Robischon, 2006).

Based on evidence of extensive conservation in photoperception and light signal transduction in angiosperms, this work aimed to identify the characterized components of these pathways in citrus. Our results have demonstrated that a large portion of the genes involved in light responses from model species are present in citrus and that they share extensive protein sequence conservation in several regions, including functionally characterized domains. These results demonstrate the potential use of comparative genomic tools to elucidate physiological and metabolic processes in crop species.

Material and Methods

Database searches and alignments

Homologs of Arabidopsis thaliana and other model species photoperception and light signal transduction genes were identified in BLAST searches (Altschul et al., 1997) against EST sequences from the citrus index databases at CitEST, consisting of approximately 176,200 ESTs obtained from the sequencing of 53 libraries. Data validation was performed by tBLASTx and tBLASTn searches using BLOSUM80 scoring matrix of the retrieved hits against the databases at NCBI (National Center for Biotechnology Information) built inside the CitEST project. Sequences failing to retrieve the original bait sequence were eliminated from the projects. The resulting alignments were filtered by a threshold e-value of 1e-15 and the validated hits were further analyzed according to functional domain description. Validated sequences were translated and protein (deduced amino acid) alignments were performed using ClustalX (Thompson et al., 1997). When necessary, alignments were manually adjusted using Lasergene MegAlign (DNASTAR, Madison, WI, USA).

Motif analysis and in silico characterization

The identified homologs were investigated for the presence and sequence conservation of recognizable functional domains described in several protein analysis and gene function databases (European Bioinformatics Institute-European Molecular Biology Laboratory - EMBL-EBI; Expert Protein Analysis System - ExPaSy from the Swiss Institute of Bioinformatics - SIB; Protein Families database - Pfam).

Phylogenetic analysis

The functionality of citrus genes in comparison to the characterized homologs was assessed by genetic distance and phylogenetic studies. Phylogenetic analyses were performed using distance and parsimony methods in the software PAUP

Results and Discussion

The genes characterized as essential players in light-controlled developmental processes in A. thaliana and other model species were compiled, including those involved in light sensing, seed germination, seedling establishment, phototropism and shade-avoidance responses. Their protein sequences were used to search citrus EST databases and the retrieved sequences were ranked according to the degree of amino acid sequence conservation and further analyzed. In this way, we have identified 102 EST contigs corresponding to genes involved in light-regulated developmental control in citrus genome (Figure 1, Figure S1). From the total, 27 ESTs and EST contigs share sequence homology with photoreceptor and putative photoreceptor families, 53 represent several phy and cry signal transduction components and light-regulated transcription factors, whereas the remaining 22 are similar to phot signaling partners (Figure 1). Homologs from the transcriptional regulators PAT1 (PHYTOCHROME A SIGNAL TRANSDUCTION 1, AT5G48150) (Bolle et al., 2000), HRB1 (HYPERSENSITIVE TO RED AND BLUE 1, AT1G02340) (Kang et al., 2005), OBP3 (OBF4-BINDING PROTEIN 3, AT3G55370) (Ward et al., 2005) and from the novel signaling components FHL (FHY1-LIKE, AT5G02200) (Zhou et al., 2005) and SRR1 (SENSITIVITY TO RED LIGHT REDUCED 1, AT5G59560) (Staiger et al., 2003) were absent from CitEST databases. However, the existence of citrus orthologs cannot be ruled out at this point due to the restricted coverage of the transcriptome analysis, the expression levels and patterns of these genes and the post-translational modifications required to generate functional components. In Arabidopsis and rice, several genes involved in light signaling have been identified by biochemical, forward and reverse genetic assays (Zhou et al., 2005; Kevei et al., 2006)

Photoreceptor-related genes

Citrus EST database contains homologs of members of all families of plant photoreceptors: namely, the phytochrome, cryptochrome and phototropin families (Table S1, Figure 2, Figure 3, Figure 4). In higher plants, phy are responsible for the control of major developmental processes, such as seed, germination, de-etiolation, shade avoidance, floral induction and entrainment of the circadian clock (Chen et al., 2004). Four EST singlets sharing sequence similarities to phy family genes were identified; three in C. sinensis and one in C. reticulata genome (Table S1). Two of C. sinensis ESTs show higher levels of sequence similarity to PHYA genes, whereas the remaining ones are related to PHYB-type of sequences. Interestingly, the PHYB homologs in citrus appear to be more distantly related from the Populus PHYB1 and PHYB2 sequences than from the A. thaliana PHYE gene (Figure 2). The branching in the PHYB genes is a relatively recent event and is absent from many plant species, including Arabidopsis (Mathews, 2006). The partial nature of the sequences prevent us from speculating whether citrus genome has a single PHYB gene or two, like the current model woody plant Populus.

The cryptochrome family is represented in the citrus genome by two ESTs corresponding to Arabidopsis CRY1 and five sequences similar to CRY-DASH (Table S1, Figure 3). Although, all the identified sequences share similarities to higher plant cry sequences, for the majority of them (five), the deduced amino acid sequence identity is restricted to the photolyase-like domain (Figure 3), indicating that these genes may function as photolyases rather than bona fide B photoreceptors. The C-terminal extension, essential for cry1 function in Arabidopsis, is conserved in C. sinensis EST and in C. reticulata EST contig (Table S1, Figure 3). Cryptochromes are mainly responsible for de-etiolation under blue light in Arabidopsis, including control of transcriptional regulation, inhibition of hypocotyls growth, promotion of cotyledons expansion, and synthesis of several non-photoreceptor pigments, such as chlorophyll and anthocyanins (Li and Yang, 2006). In addition, this class of photoreceptor acts in coordination with phy to reset the circadian clock and to control the transition to flowering (Yanovsky and Kay, 2002). At least two of the identified sequences (CS00-C1-100-038-A12.CT and C13-CA) are likely to code for functional cry family members in citrus.

In Arabidopsis, the phototropin photoreceptor family consists of two closely related members that share almost 60% protein identity. In the genome of citrus species, an EST contig whose deduced amino acid sequence shows 71% identity to PHOT2 and four cDNAs with sequences approximately 50% identical to PHOT1 and PHOT2, were identified (Figure 4A, Table S1). The overall sequence conservation between citrus and other species PHOT proteins is high, including at the N-terminal LOV domains, essential for chromofore binding and protein function in Arabidopsis, reviewed in Quecini and Liscum (2006). The remaining identified ESTs and EST contigs present high levels of sequence identity restricted to the C-terminal serine/threonine kinase and thus, may not perform photoperception-related functions. In Arabidopsis and rice, phot family controls a specific sub-set of physiological processes, including phototropic stem curvature, stomata opening control and chloroplast relocation (Quecini and Liscum, 2006). Only recently, phots have been demonstrated to be involved in B-mediated seedling de-etiolation (Folta et al., 2003; Takemyia et al., 2005). In Arabidopsis, phot1 and phot2 have specialized and overlapping roles, phot1 being the most important photoreceptor sensing directional B under low fluence rates and phot2 responsible for high light responses (Briggs and Christie, 2002). The presence of multiple PHOT-like sequences in citrus genome suggests that such a fluence rate-specific role might occur.

Recently, a three-member family of putative photoreceptors has been characterized in Arabidopsis; the ZTL/FKF1/LKP2 family (Somers, 2001). It is represented by three distinct sequences in citrus genome databases: one highly similar to FKF1 with lower homology to ZTL and two sharing sequence similarity to FKF1 and LKP2 (Table S1, Figure 4B). Arabidopsis ZTL/FKF1/LKP2 proteins are characterized by the presence of a flavin-binding LOV domain at the protein N-terminal, an F-box domain and a stretch of Kelch repeats, providing a direct link between light perception and ubiquitin-mediated protein degradation. The family has been functionally associated to the endogenous time-keeping mechanism and the control of photoperiodic flowering time (Imaizumi et al., 2003; Imaizumi et al., 2005). In Arabidopsis, ZTL and FKF1 are thought to be components of an Skp1-Cullin-F-box (SCF) E3 ubiquitin ligase complex (Vierstra, 2003). ZTL has been implicated in the ubiquitin-mediated proteolytic degradation of the clock component TOC1 (Más et al., 2003) and in the regulation of developmental responses to R, possibly through its interaction with phyB (Kevei et al., 2006), while FKF1 has been demonstrated to control the levels of the photoperiod-sensing CONSTANS (CO) gene via degradation of its transcriptional repressor, a DOF type transcription factor, CDF1 (Imaizumi et al., 2003; Imaizumi et al., 2005). Thus, ZTL post-translationally regulates TOC1 levels and FKF1 controls daily CO expression in part by degrading CDF1. Citrus FKF1/ZTL- and LKP2-like EST contigs are highly conserved at the F-box and Kelch repeats domains (Figure 4B), suggesting a function in the protelolytic degradation of circadian-clock associated factors.

Phy and cry signal transduction components

Phytochrome responses are associated with changes in gene expression (Casal and Yanovsky, 2005) and members of several transcription factor families are required for phy signaling or are early targets of phy-mediated responses. In citrus, 22 EST contigs corresponding to the Arabidopsis transcriptional regulators and nuclear factors involved in phy and cry light signaling were identified, along with 17 transcripts associated to light-mediated proteolysis and seven transcripts similar to several signaling events of light signaling, such as Ca²⁺-binding and post-translational protein modification (Figure 1, Table S2).

In Arabidopsis, the PIF (PHYTOCHROME-INTERACTING FACTOR) and PIL (PIF-LIKE) family of bHLH (basic Helix-Loop-Helix) transcriptional regulators, which includes HFR1/REP1/RSF1 (LONG HYPOCOTYL IN FAR RED 1/REDUCED PHYTOCHROME SIGNALING 1/REDUCED SENSITIVITY TO FAR-RED LIGHT 1), is one of the best-characterized phy signaling partners (Quail, 2002). PIF3 interacts with the R-activated form of phyA and phyB in a conformation-specific manner (Ni et al., 1999) and binds specifically to a cis-acting regulatory element (G-box) in the promoters of several phytochrome-responsive genes. Simultaneous binding of PIF3 to promoters of light-responsive genes and to the Pfr form of phyB (Martinéz-Garcia et al., 2000) indicates that PIF3 recruits phyB to the promoters of actively transcribed genes (Figure 5A). Moreover, PIF3 can heterodimerize with other bHLH proteins, such as HFR1 (Fairchild et al., 2000) and PIF4 (Huq and Quail, 2002). Thus, the current hypothesis for PIF/PIL function in Arabidopsis is that: (i) phytochromes, mainly phyA, act through PIF3 and other yet unidentified factors to regulate transcription of a master set of regulators, such as CCA1 (Wang and Tobin, 1998), LHY1 (Schaffer et al., 1998), TOC1 and CO (Harmer et al., 2000; Tepperman et al., 2001); and (ii) these regulators then control the transcription of genes encoding functions necessary for the terminal steps of the signaling cascade. Interestingly, in citrus genome databases, the PIF/PIL/HFR family is represented by a single EST contig from C. aurantifolia and C. latifolia, displaying higher identity to PIF4 and HFR1 protein (Table S2, Figure 5). Another two highly similar EST contigs (55.5% deduced amino acid sequence identity) showed moderate (15.0 to 17.5%) and low (7.5 to 2.9%) identity to HFR1 and PIF/PIL gene products, respectively. The functional significance of these transcripts as PIF/PIL/HFR-like light-induced transcriptional regulators remains unclear. The absence of PIF-like transcripts in C. sinensis and C. reticulata transcriptomes, which together correspond to approximately 72% of CitEST database, is noteworthy given their importance in light-mediated responses in Arabidopsis.

Several basic domain/zinc finger (Zn finger) and MYB-type factors function as downstream convergent targets of phy and cry signaling in Arabidopsis, independently of G-box photoreceptor binding (Oyama et al., 1997; Chattopadhyay et al., 1998; Ballesteros et al., 2001). In citrus species transcriptome, six cDNAs corresponding to this class of transcriptional regulators were present: namely, one HY5 (LONG HYPOCOTYL 5), one HYH (HY5-HOMOLOGOUS) and four LAF1 (LONG AFTER FAR RED 1) homologs (Table S2, Figure 6A). Down-regulation of these signaling pathways occurs when phyA and the transcription factors, HY5 and LAF1, are degraded in a light-dependent fashion by the proteasome in a mechanism that involves COP1 (CONSTITUTIVELY PHOTOMORPHOGENIC 1) (Saijo et al., 2003; Seo et al., 2004; Jang et al., 2005). The COP9 signalosome (CSN) is also involved in HY5 degradation (Peng et al., 2001). Moreover, SPA1 (SUPRESSOR OF PHYA-105 MUTATION) and the other members of the SPA family regulate the ubiquitin-ligase activity of COP1 (Saijo et al., 2003; Seo et al., 2003). In citrus EST databases, COP1, other components of the CSN and a small group of SPA-like transcripts were identified, suggesting the existence of a similar mechanism of phy-mediated signal desensitization route (Table S2, Figure 6B).

Photoreceptor-initiated signaling pathways also consist of cytosolic components in Arabidopsis and other model species. General transduction pathways, such as G-protein, Ca⁺²-calmodulin and protein phosphorylation cascades have been demonstrated to take part in light-triggered signaling (Bowler et al., 1994). Homologs of several Ca⁺²-binding and protein phosphorylation factors in phy- and cry-initiated signal transduction were identified in citrus transcriptome (Table S2). Phosphorylation may be responsible for the fine tuning of light signal transduction at several checkpoints, including the degradation of active phyA mediated by the ubiquitin/26S proteasome pathway; the interaction of light-signaling positive factors with COP1, an E3 ubiquitin-protein ligase functioning as a negative regulator of photomorphogenesis (Seo et al., 2004), reducing the affinity of phosphorylated phyA to its signaling partners (Kim et al., 2004) and controlling the phosphorylation level and, consequently, the signaling activity, of phy (Ryu et al., 2005). Extensive functional conservation in angiosperms phosphorylation and post-translational protein modification suggests that the transcripts identified in citrus are involved in the proteolytic degradation of light-signaling components.

Phot signal transduction components

Phototropin-mediated signaling involves several families of transducing partner proteins. NPH3 and RPT2 are members of the 32-gene NRL (NPH 3 and RPT2-LIKE) family in Arabidopsis (Quecini and Liscum, 2006). Nine citrus EST contigs whose deduced amino acid sequences share high homology to NPH3 and RPT2 were identified (Table S3). Moreover, 12 cDNAs with the conserved N-terminal signature BTB/POZ (BRIC-À-BRAC, TRAMTRACK AND BROAD COMPLEX/POXVIRUS AND ZINC FINGER) domain and C-terminal coiled-coil, respectively, were found. The differential growth of plant organs relative to a B-light stimulus is triggered by phot directional light sensing and hypothesized to be brought about by differential auxin concentration or activity (review in Quecini and Liscum, 2006). The relocation of PIN family auxin transporters has been associated to phot-mediated stem curvature response (Friml et al., 2002; Friml, 2003). The ARF transcriptional activator, NPH4, represent a connection between auxin-mediated asymmetric growth and phototropism, indicating that phototropism requires an auxin-regulated transcriptional response (Harper et al., 2000; Tatematsu et al., 2004). Recently, NPH4/ARF7 has also been implicated in leaf expansion and auxin-induced lateral root formation in Arabidopsis (Wilmoth et al., 2005). The citrus genome databases have two EST contigs and one singlet corresponding to Arabidopsis PIN1 and PIN3 and two, highly similar to NPH4/ARF7 (Table S3), that are likely to be functionally equivalent to their Arabidopsis counterparts due to extensive identity. Phot-mediated B light perception involves H⁺-ATPase phosphorylation and association with 14-3-3 proteins in stomatal guard cells (Kinoshita and Shimazaki, 2002, Fuglsang et al., 2003). At this point, the function of the 14-3-3 family proteins remain elusive, although they have been shown to be required for H⁺-ATPase activity induced by B light (Fuglsang et al., 2003). Four citrus EST contigs showing more than 50% deduced amino acid identity to 14-3-3 proteins were identified; however, their association to phot-mediated signal transduction remains to be determined.

Concluding Remarks

This preliminary survey of citrus photoperception-associated genes has provided useful information for further studies of light developmental control in these species. It has allowed the identification of conserved members of light-triggered signaling in a non-model species and the elaboration of a work model frame for light perception and signaling in citrus (Figure 7). These prospects are particularly attractive considering the range of economically important physiological processes of citrus that are regulated by light, including secondary metabolism regulation and shading responses. An immediate goal of plant genomics is to transfer knowledge between model and crop species, allowing a better understanding of the mechanisms underlying several aspects of plant physiology. Thus, genomic and functional information can be integrated into the accumulated knowledge of citrus genetics and physiology to advance basic and applied research. These studies will help to elucidate the molecular basis of developmental plasticity and to understand how environmental factors modulate plant development and the expression of phenotypic characters. The results obtained provide a new perspective on several aspects of light-regulated physiological processes in citrus, such as de-etiolation, seedling establishment and shade-avoidance response.

Internet Resources

Supplementary Material

The following online material is available for this article:

Table S1

Table S2

Table S3

^{Supplemental Reference}

This material is available as part of the online article from http://www.scielo.br/gmb.

Received: July 21, 2006; Accepted: February 8, 2007.

Associate Editor: Alessandra Alves de Souza

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*

4.0b10, using the software default parameters. Re-sampling bootstrap trees containing 1000 random samples were constructed using PSIGNFIT software. Modular functional domains were employed for genetic distance studies for genes previously described as having divergent regions and conserved blocks.

Publication Dates

• Publication in this collection
  26 Nov 2007
• Date of issue
  2007

History

• Received
  21 July 2006
• Accepted
  08 Feb 2007