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Identification of Photoperception and Light Signal Transduction Pathways in Citrus

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Identification of Photoperception and Light Signal Transduction Pathways in Citrus Genetics and Molecular Biology, 30, 3 (suppl), 780-793 (2007) Copyright by the Brazilian Society of Genetics. Printed in Brazil www.sbg.org.br 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. 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 func- tionally 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 cy- toplasmic proteins mediating photoreceptor-induced responses although some important Arabidopsis phytochrome- and cryptochrome-signaling components are absent from citrus sequence databases. The main gene families re- sponsible for phototropin-mediated signal transduction were present in citrus transcriptome, including general regu- latory 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 iden- tified 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. Received: July 21, 2006; Accepted: February 8, 2007. Introduction al., 2001; Somers et al., 2000). ZTL/ FKF1/LKP2 are in- Plant development is highly plastic, allowing the envi- volved in the circadian clock mechanism and photoperiodic ronment to exert tight control over the transitions between flowering response (Imaizumi et al., 2005). genetic developmental programs in order to maximize In higher plants, photoreceptor co-action is a com- growth and reproduction (Meyerowitz, 2002). Light pro- mon theme and the pathways may function synergistically, vides spatial and temporal information to regulate plant de- antagonistically and additively to control several develop- velopment throughout its life cycle: from germination and mental responses (Schäfer and Nagy, 2006). Moreover, seedling establishment to the onset of the reproductive stage plant photoreceptors operate in concert with numerous (Schäfer and Nagy, 2006). Plants are able to detect environ- other signaling systems; including phytohormones, carbo- mental light direction, duration, fluency and wavelength due hydrate-mediated, temperature, gravity and the endoge- to a complex system of photoreceptor molecules: the blue nous clock transduction pathways (Halliday and (B) and ultraviolet-A (UV-A) 320-500 nm light-sensing Fankhauser, 2003; Chen et al., 2004; Heggie and Halliday, cryptochromes (cry) and phototropins (phot) (Banerjee and 2005). The molecular mechanisms involved in light- Batschauer, 2005) and the red (R)/far red (FR) 600-750 nm induced signal transduction include the following: light-re- phytochrome (phy) receptors (Schepens et al., 2004). Re- gulated sub-cellular localization of the photoreceptors cently, a novel family of putative B photoreceptors has been (Guo et al., 1999; Nagy and Schäfer, 2002; Chen et al., described in Arabidopsis thaliana: the ZEITLUPE (ZTL)/ 2005; Kong et al., 2006); a large reorganization of the Flavin-binding Kelch repeat F-box protein (FKF1)/LOV transcriptional program (Casal and Yanovsky, 2005; Fran- Kelch Protein (LKP2) family (Nelson et al., 2000; Schultz et klin et al., 2005) and light-regulated proteolytic degrada- tion of several photoreceptors and signaling components Send correspondence to Vera Quecini. Centro de Pesquisa e (Höcker, 2005; Huq, 2006). Desenvolvimento de Recursos Genéticos, Instituto Agronômico de Campinas, Caixa Postal 28, 13001-970 Campinas, SP, Brazil. Studies employing model plant species have demon- E-mail: [email protected]. strated that photoperception, the signal transduction path- Quecini 781 ways and the responses elicited by light form a complex were identified in BLAST searches (Altschul et al., 1997) interconnected network rather than a linear pathway (Chen against EST sequences from the citrus index databases at et al., 2004; Quecini and Liscum, 2006). The diversity of CitEST, consisting of approximately 176,200 ESTs ob- light responsiveness observed in plants has arisen from the tained from the sequencing of 53 libraries. Data validation elaboration, combination and re-arrangement of a basic was performed by tBLASTx and tBLASTn searches using repertoire of mechanisms responsible for light-mediated BLOSUM80 scoring matrix of the retrieved hits against the developmental regulation, allowing adaptation to a wide databases at NCBI (National Center for Biotechnology In- range of climatic and latitudinal regions. Comparative formation) built inside the CitEST project. Sequences fail- genomics has provided tools to access the genetic bases of ing to retrieve the original bait sequence were eliminated this diversity in non-model species using bioinformatics, from the projects. The resulting alignments were filtered by which increases the fundamental knowledge of gene inter- a threshold e-value of 1e-15 and the validated hits were fur- actions and permits analyses of the functional significance ther analyzed according to functional domain description. of proteins in silico (e.g. Santelli and Siviero, 2001; Souza Validated sequences were translated and protein (deduced et al., 2001; Hecht et al., 2005). amino acid) alignments were performed using ClustalX Virtually all information about light-regulated devel- (Thompson et al., 1997). When necessary, alignments were opment in woody plants comes from studies with Populus,a manually adjusted using Lasergene MegAlign temperate deciduous perennial (Zhu and Coleman, 2001; (DNASTAR, Madison, WI, USA). Olsen and Juntilla, 2002). Adaptive traits in temperate peren- Motif analysis and in silico characterization nial woody plants involve an integrated physiological re- sponse directed at plant survival and nutrient storage over the The identified homologs were investigated for the winter period and are greatly dependent of photoreceptor- presence and sequence conservation of recognizable func- mediated perception of seasonal progression (Thomas and tional domains described in several protein analysis and Vince-Prue, 1997). Surprisingly, recent evidence has dem- gene function databases (European Bioinformatics Insti- onstrated that light is also the main factor triggering the tran- tute-European Molecular Biology Laboratory - EMBL- sition between vegetative to reproductive developmental EBI; Expert Protein Analysis System - ExPaSy from the stages of trees in Equatorial regions (Borchert et al., 2005). Swiss Institute of Bioinformatics - SIB; Protein Families The effects of light on developmental processes in citrus and database - Pfam). other neotropical tree species have been described in several situations, although without approaching the molecular as- Phylogenetic analysis pects of the metabolism (Steppe et al., 2006; Chen L-S et al., The functionality of citrus genes in comparison to the 2005; Raveh et al., 2003; Torné et al., 2001). Mutant studies characterized homologs was assessed by genetic distance employing transgenically generated plants have demon- and phylogenetic studies. Phylogenetic analyses were per- strated variable extents of functional conservation in the formed using distance and parsimony methods in the soft- genes responsible for developmental control between citrus ware PAUP* 4.0b10, using the software default parame- and model species (Pena et al., 2001; Pillitteri et al., 2004). ters. Re-sampling bootstrap trees containing 1000 random However, the detailed functional characterization of individ- samples were constructed using PSIGNFIT software. Mod- ual genes is a limiting factor in the study of tree species, and ular functional domains were employed for genetic dis- new strategies should be devised for the study of gene func- tance studies for genes previously described as having di- tion (Groover and Robischon, 2006). vergent regions and conserved blocks. Based on evidence of extensive conservation in photo- perception and light signal transduction in angiosperms, this Results and Discussion work aimed to identify the characterized components of these The genes characterized as essential players in light- pathways in citrus. Our results have demonstrated that a large controlled developmental processes in A. thaliana and portion of the genes involved in light responses from model other model species were compiled, including those in- species are present in citrus and that they share extensive pro- volved in light sensing, seed germination, seedling estab- tein sequence conservation in several regions, including func- lishment, phototropism and shade-avoidance responses. tionally characterized domains. These results demonstrate the Their protein sequences were used to search citrus EST da- potential use of comparative genomic
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