Molecular Mechanisms of Phytochrome Signal Transduction in Higher Plants

Colloids and Surfaces B: Biointerfaces 45 (2005) 154–161

Molecular mechanisms of phytochrome signal transduction in higher plants

Li-Ye Chu a,b,1, Hong-Bo Shao a,b,c,∗,1, Mao-Yau Li a

a Molecular Biology Laboratory, Bio-informatics College, Chongqing University of Posts & Telecommunications, Chongqing 400065, PR China b Biological Laboratory, Chemical Engineering College, Qingdao University of Science and Technology, Qingdao 266042, China c The State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, The Centre of Soil and Water Conservation and Eco-environmental Research, The Chinese Academy of Sciences and Northwest Sci-tech University of Agriculture and Forestry, Yangling 712100, PR China

Received 9 May 2005; accepted 28 May 2005

Abstract

Phytochromes in higher plants play a great role in development, responses to environmental stresses and signal transduction, which are the fundamental principles for higher plants to be adapted to changing environment. Deep and systematic understanding of the phytochrome in higher plants is of crucial importance to molecular biology, purposeful improvement of environment in practice, especially molecular mechanism by which higher plants perceive UV-B stress. The last more than 10 years have seen rapid progress in this ﬁeld with the aid of a combination of molecular, genetic and cell biological approaches. No doubt, what is the most important, is the application of Arabidopsis experimental system and the generation of various mutants regarding phytochromes (phy A–E). Increasing evidence demonstrates that phytochrome signaling transduction constitutes a highly ordered multidimensional network of events. Some phytochromes and signaling intermediates show light-dependent nuclear-cytoplasmic partitioning, which implies that early signaling events take place in the nucleus and that subcellular localization patterns most probably represent an important signaling control point. The main subcellular localization includes nucleus, cytosol and chloroplasts, respectively. Additionally, proteasome-mediated degradation of signaling intermediates most possibly function in concert with subcellular partitioning events as an integrated checkpoint. What higher plants do in this way is to execute accurate responses to the changes in the light environment on the basis of interconnected subcellular organelles. By integrating the available data, at the molecular level and from the angle of eco-environment, we should be able to construct a solid foundation for further dissection of phytochrome signaling transduction in higher plants. © 2005 Elsevier B.V. All rights reserved.

Keywords: Phytochrome; Higher plants; Molecular biology; Signal transduction; An ordered multidimensional network

1. Introduction of events [1–4,30,37,42]. Light is one of the most important eco-environmental factors affecting higher plant growth, Phytochrome signal transduction in higher plants has often development and gene expression-control at the molecular been regarded as a non-spatially separated linear chain of level [16,37,41]. Higher plants respond to light in different events for the past 50 years. But a tight combination of ways ranging from simple signal perception and execution molecular, genetic and cell biological approaches have lead in single-cell prokaryotes to complicated signaling networks to current realization that phyrohrome signaling pathways in multi-cellular eukaryotes [1,29,40] (Bonioltti et al., 2002; are composed of a highly ordered multidimensional network Shao et al., 2004). Light not only functions as the most important energy source for photosynthesis, but higher plants have

∗ to monitor the light quality and quantity input for the sake of Corresponding author. Tel.: +86 29 87011190/23 62477654; executing the corresponding physiological and developmen- fax: +86 23 62460025/29 87012210. E-mail address: [email protected] (H.-B. Shao). tal responses. To reach this end, higher plants have evolved a 1 The authors contributed to this paper equally. complex set of photoreceptors, which include the blue/UV-A

0927-7765/$ – see front matter © 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.colsurfb.2005.05.017 L.-Y. Chu et al. / Colloids and Surfaces B: Biointerfaces 45 (2005) 154–161 155 absorbing cryptochromes and the red/far-red light absorbing phytochromes [5]. The knowledge about the roles of phytochrome action is relatively complete, however, the insight into how the per- ceived light signals are transduced leading to morphological responses and altered gene expression patterns has remained somewhat sparse [1]. More recently, the isolation of mutants Fig. 1. Structural features of phytochrome B protein, indicating the positions of the chromophore attachment site, serine phosphorylation sites, histidine disrupted in genes encoding phytochrome signaling interme- kinase-related domains (HKRD) and the two PAS domains [1,22,36,37]. diates have identified both positive and negative components of these phytochrome signaling pathways. In addition, using protein–protein interaction technology, such as yeast two-hybrid and in vitro pull-down assays, there have been red reversible plant responses. It has since been clear that exciting advances in understanding the plethora of physical phytochromes belong to closely related family of photore- interactions that take place not only between phytochrome ceptors, the apoproteins of which are encoded by a small and early signaling intermediates but also between bona fide family of divergent genes. Arabidopsis thaliana has five dis- signaling components [5–11]. An emerging viewpoint from crete apophytochrome-encoding genes, PHYA-PHYE, iso- the available data is that phytachrome signal transduction in lated and sequenced [23–25]. Arabidopsis PHYB and PHYD higher plants is a highly ordered but yet complex network polypeptides are approximately 80% identical and are more of events with different branches of the signaling network closely related to PHYE than they are to either PHYA or spatially separated into different subcellular compartments PHYC (approximately 80% identity) [27,28,37]. Counter- (Xiong et al., 2001) [22]. Moreover, several other nuclear parts of PHTA, PHYB and other PHY genes are present in phytochrome signaling components have been identified most, it not all, higher plants. clearly implying that the nucleus is a hot-spot for early All of the higher plant phytochromes appear to share the signaling events [1,5]. Nowadays, there have been a larger same basic structure, consisting of a dimmer of identical number of components that we need to integrate at the whole 124 kDa polypeptides. Each monomer carries a single cova- cell level to further understand phytochrome signal transduc- lently linked linear tetrapyrrole chromophore (phytochromo- tion. It is evident that many organelles are actively involved bilin), attached via a thieother bond to a conserved cysteine in phytochrome signaling and that these organelles are residue in the N-terminal globular domain of the protein. interconnected [12,13,26]. It is also clear that the subcellular The C-terminal domain encompasses two histidine kinase- partitioning of both phytochrome and signaling intermediates related domains (HRKD) and two motifs with homology to provides an elegant controling mechanism. Likewise, the PAS (PER-ARNT-SIM) domains [9,10,14,37]. PAS domains finely tuned degradation of signaling pathway components are present in various signal transduction molecules which by the 26s proteasome is clearly an important checkpoint sense environmental signals, such as light conditions, oxy- [14,15,30–32]. Additionally, the multitude of interactions gen levels and redox potential [1]. They may also mediate that occur among phytochrome signaling pathways is very protein–protein interaction (Fig. 1). The amino terminal half attractive and these interactions depend on controlled subcel- of phytochromes can be considered as a light sensing dor- lular partitioning events [1,17,18]. This paper focuses on the main whist the carboxyl-terminal half can be regarded as the molecular biology of phytochrome signaling transduction regulatory domain (Fig. 1). in higher plants in terms of components of its different Higher plant phyrochrome can be classified into two pathways, the overall phytochrome signaling network and groups based on the stability in light: type I (phy A) occurs main existing problems in this frontier area. It is an accepted in etiolated tissues in large quantities and is subject to a fact that one of the keypoints to further dissect phytochrome high turnover, i.e., is light labile and type II (phy B–phy signal transduction is to use the spectrum of molecular E), are light stable. Higher plant phytochromes undergo and biochemical tools available, not only to isolate new photoconversion between two stable states: the red light signaling components, but also to integrate the pool of phy- absorbing form (Pr, synthesized in the dark) and the farred tochrome knowledge in a cellular and molecular biological light absorbing form (Pfr). This Pr-to-Pfr transition is due context. to a light induced double bond rotation in the chromophore and rearrangements of the protein backbone of the apoprotein. For most responses Pfr is considered to be the bio- 2. Basic structure and functions of phytochromes in logically active form. The Pr forms of (at least some) higher plants phytochromes of higher plants localize to the cytoplasm, whereas a proportion of the Pfr (active) isofoms localize 2.1. Basic structure to the nucleus [19]. To put phytochrome signaling in biological content, the authors will briefly describe the prin- Higher plant chromes were first described by Borthwick cipal biological functions of higher plant phytochromes as et al. (1952) as the receptors responses [1,36], for red/far- follows. 156 L.-Y. Chu et al. / Colloids and Surfaces B: Biointerfaces 45 (2005) 154–161

2.2. Primary functions ever, it was later shown that cry1 had biological activity in a phy A phy B null mutant background in blue light, Phytochrome A (phy A) is responsible primarily for sens- especially at higher fluence rates [39]. Cryptochromes and ing prelonged farred light in the farred. High irradiance phytochromes also interact in phototropic curvature: prior response (HIR) mode of phytochrome action. This response stimulation of phytochrome red light enhances the blue light- mode operates in the regulation of many aspects of seedling mediated response, and this appears to be regulated by phy de-etiolation, including inhibition of hypocotyls elongation, A [36]. Additionally, phy B and cry 2 act antagonistically in the expansion of cotyledons, changes in gene expression regulating flowering: phy B appears to repress whilst cry 2 and the synthesis of anthocyanin, etc. (Porta et al., 2003) stimulates floral induction [9]. In addition to these genetic [15,16,35]. These responses to prolonged far red irradiation studies indicating interactions between phytochromes and are absent in phy A null seedlings. Phytochrome A also cryptochromes there is also evidence that cry1 can physi- mediates the very low fluence responses (VLFR) of etio- cally interact with phy A in yeart-two-hybrid assays and more lated seedlings. In addition, in both young seedlings and in recently that cry 2 can interact with phy B. Some results mature Arabidopsis, phy A appears to be more important from the laboratory of the authors demonstrated further by for perception of daylength [36,37]. Phytochrome B (phy experimenting with barley matured seeds and embryos that B) deficiency leads to impaired de-etiolation responses in endogenous hormones, in particular, ABA, in conjunction red light, but not in prolonged far-red, thus, it is concluded with phytochrome A, cryptochrome 2 affected the charac- that for de-etiolation responses, phy A and phy B have dis- ter of the explants cultured in vitro; implying that there is crete photosensory activities. Phytochrome B also plays a an interconnected signal transduction network among phy- major role in the low fluence response (LFR) and promo- tochromes, cryprochromes, phytohormones and environmen- tion of seed germination, which is a red/far-red responsible tal stresses [33,35–39,41] (Shao et al., 2002). response [1]. Phyrochrome B is considered to be the main phytochrome responsible for the shade avoidance response as phy B-deficient mutants have the typical architecture 3. Higher plant phytochrome signaling components of the mature light-grown plant displaying shade avoid- and their localizations ance responses (elongated grocoth habit, reduced leaf area, increased apical dominance and early flowering, [14,36,37]). Upon photoconversion from Pr to Pfr, the phytochrome This indicates that phy B perceives the low red/far-red sig- rapidly induces a cascade of signaling events, during which nals, which result from the far-red-rich light that is reflected the signaling components and localization play greater func- from (or transmitted through) the leaves of nearby plants. tions. Combining some work from my laboratory with the From analyses of various phytochrome mutant combina- recent literature, main phytochrome signaling components tions, it is clear that both phy D and phy E are also mediators and their subcellular localizations are summarized in Table 1. of shade avoidance responses, such as petiole elongation and flowering time, with phy E having a specific role in regu- 4. Interactions between higher plant phytochromes lating internode elongation. Phy E also, plays a role in the and their signaling pathways red/far-red reversible promotion of seed germination and in the promotion of germination by far-red light, a response pre- Signal transduction pathways have often been viewed as viously considered to be mediated solely by phy A. Studies of linear chain of events but it is becoming increasingly clear phy C functions have previously relied on analysis of trans- that there is extensive cross-talk between different pathways genic plants that over-express phy C and analysis of the phy [1,20]. Many interactions involve modulating various path- A, phy B, phy D, phy E quadruple mutant [16,22,23]. These way inputs, by which higher plants can develop in response studies have revealed that phy C may play a role in regulat- to changing environmental and developmental hints. The ing leaf expansion and in the perception of daylength, but isolation of hormone signaling mutants and the recent char- that phy C appears not to play a major role in responses to acterization of key regulatory processes have given extensive low red/far-red ratio [1,36,37]. insight into how light and hormone signaling are integrated Many studies from the analyses of Arabidopsis mutants and regulated harmoniously [21,36,37] (Shao et al., 2002). containing null alleles of one or more phytochromes have It is a clear fact that hormones contribute to photomor- been carried to try to dissect the individual roles of phy- phogenic responses in that both light and hormones generally tochromes. However, this is often complicated because as act on similar cells and organs involving cell elongation and well as having independent functions, phytochromes also other reactions whilst auxin, brassinosteroids and GA stimu- show redundancy of functions and may modulate the action late cell elongation with each having some special roles. of each other. Clearly, phytochromes also interact and coact with other photo eceptors [36,37]. 4.1. Auxin Cashmore (1997) reported that cryptochrome action, in the inhibition of hypocotyl elongation under blue light, was The functions of auxin during higher plant development dependent upon the presence of phy A or phy B. How- involve many aspects. At the tissue and organ level, auxin is L.-Y. Chu et al. / Colloids and Surfaces B: Biointerfaces 45 (2005) 154–161 157

Table 1 Main phytochrome signaling components and their subcellular localizations in higher plants [1,5,8,35–37,39–41] Mutant Phenotype of Mutant Protein Interaction Nucleus, Poc 1 Hlypersensitive for red induced de-etiolation PIF3, Similarities to b-HLH transcription Phy A & Phy B SN, Phy A & factors; promoter insertion causing Phy B in Y2H increased levels of PIF3 Gi-100 Impaired response to ed GIGANTEA, Circadian clock-controlled PhyBSN gene that regulates photoperiodic flowering sf1/hfr/res rsf1: creduced senstivsty to far-red; hfrl (long RSF1/HFR1/REP1, Similarities to b-HLH PhyASN hypocofyl in far-red); rep1; (reduced franscription factors; high sequence identity phytochrome signallig1) to PIE3 Far 1 Impaired response to far-red FAR1, Putative coiled-coil domain Phy A SN Spa 1 Isolated as a suppressor of weak phy A SPA1, WD repeat prctein ELF3 Phy A SN, Cop1 in Y2H mutation Elf 3 Early flowring Circadian clock-regulated protein Phy B SN Hy 5 Impaired responses to farred, Red and blue HY5, BZIP transcription factor Cop1 in Y2H light Shy 2 Shy2-ID and Shy 2-2, Suppreors of the IAA3 Auxin-induced, Transcription factor Phy A SN, copreciptation long-hypocotyl, Phenotype of hy2 and hy3, with phy B protein respectively Cytosol, Pat 1 Insensitive to far-red PAT 1, VHIID/GRAS Protein Phy A SN Fin219 Impaired response to far-red FIN219, Auxin-inducible GH3 Protein Phy A SN, FHYI interaction by genetic analysis PkS1 PkS1 overexpression; impaired, response to PKS, phytochrome kinase, Substrate 1 Ionby geretic, Analysis, Phy red; PKS1 antisense, Lines: no effecton plant BSN,PhyA&PhyBin Phenotyp-e Y2H Chloroplast Impaired response to farred LAF6, ABC-like protein Phy A SN Gun5 Pale leaves: nuclear Lhcb1, Expression in the GUN5: ChlH subunit, Of Mg-chelatase Hyland GUN5, Metabolic absence of, chlorolast development inter, action SN, signaling network; YTH, yeast-two-hybrid screen. involved in root elongation, lateral root development meris- embryos cultured in vitro (Shao et al., 2002). The main dif- tem maintenance and senescence while at a cellular level ficulty in the elucidation of the CTK signaling pathway is this hormone is concerned about cell division, cell differ- the scarcity of target genes that are induced specifically by entiation and cell elongation [38,39,41] (Shao et al., 2002). the mutation. To date, three genes, IBC6, IBC7 and Cyc3 Early studies into auxin signaling mainly concentrated on appear to be primary targets of CTK since their induction the identification of auxin responsive DNA sequence ele- can occur without new protein synthesis. CTK and light can ments. A sum of auxin regulated genes have been isolated clearly elicit similar physiological and biochemical reponses and the recent use of Arabidopsis mutants has started to bring and recentest progress has started to untangle the complexity out the auxin hatchway and its interaction with phytochrome of this interaction [1,26,27]. Another finding that chloro- signaling [1,36,37]. Many results strengthen the hypothesis plasts contain a wide range of CTKs and enzymes needed that the nucleus is not the early subcellular compartment that for their metabolism has also provided a link between light contains auxin light pathway integrators. Deng et al. (2000) and CTK signaling [26,27]. Very recently, it has been shown have demonstrated that fin 219 exhibits far red light induced that CTK can rescue photomorphogenic responses in the pea hypocotyl elongation. Fin 219 was modulated as a suppresser lip 1 mutant. By adding CTK to both the lip 1 mutant and of COP1 and the disrupted gene encodes an auxin-inducilote wild type seedlings in darkness phy A levels were reduced cytoplasm protein with good homolgy to GH3-like proteins. in both lip 1 and wild type. Harter (University of Freidsburg, No doubt, it is obvious that auxin play a major function in Germany) reported on the interaction of the response regula- various developmental processes, both at the physiological tor protein ARR4 with phy B in the meeting of January 2002 and molecular level, and that a number of these processes are Keystone Symposium in Tahoe City, CA, USA. Response modulated through phytochrome actions. regulators are part of a conserved multistep phosphorylation signaling mechanism in eukaryotes. ARR4 was found to 4.2. CTK interact with the extreme N-terminus of phy B and to modulate phy B response in a phosphorytation-dependent manner. CTKs regulate many developmental processes including Higher plants overexpressing ARR4 displayed enhanced sen- activation of all division, suppression of apical dominance sitivity to red light, where Spm-insertion ARR4 knockout and senescence, inhibition of root growth and stimulation of higher plants and these expressing a ponphosphorylation de-etiolation. An appropriate proportion of CTK to auxin ARR4 showed reduced red light sensitivity. ARR4 expres- (IAA) can result in the rise of callus of barley matured sion was induced by CTK as well as red light, suggest- 158 L.-Y. Chu et al. / Colloids and Surfaces B: Biointerfaces 45 (2005) 154–161 ing its involvement in regulating the interactions between under drought stress. Some results from our laboratory sup- light and hormones. Signaling pathways [26,27]. The chro- ported the aboved evidence [33] (Shao et al., 2002). the mophore domain of phytochrome (especially the N-terminal ABHI gene was found to encode a nuclear RNA cap bind- region, where ARR4 binds phy B) undergoes major struc- ing protein that functions in RNA processing [26,27]. ABHI tural change during photoconversion. Manzawa (Reitachi is speculated to act as a modulator of ABA signaling by Advanced Research Laboratory, Saitama, Japan), together influencing transcript processing of early ABA signaling reg- with Fusaya and colleagues, is investigating the hypothe- ulatory factors [24] some results of what were reported in sis that chromophore structure determines the photosensory literature strengthen this proposal. Another ABA signaling specificity of phy A and phy B. Chromophore and phy- protein with a putative function in RNA splicing is SADI, cocyanobilin were supplied exogenously to phy A phy B which was discovered by Zhu (University of Arizona). The chromophore-deficient double mutants; it was found that sadi (supersensitive to ABA and drought) mutant shows ABA phy B-mediated responses were restored by both synthetic hypersensitive seed germination and increased expression of chromophores, whereas phy A-mediated responses occurred the luxciferase reporter under the control of the ABA respon- only when phytochromoblin was supplied. Phycocyanobilin sive promoter r29A. SADI encodes a protein that is similar appears to lack the capacity for interaction with a specific to a component of the splicesome in humans, suggesting amino acid of the phy A apoprotein. Stanzas also reported on that SADI may affect ABA responses to ROS metabolite the translocation of phy A and phy B into the nucleus dur- [22–24]. ing the light response, which appears to be a common step in phytochrome signaling. Stanzawa and colleagues detected 4.4. GAs some immunocytochemical differences between the phy A and phy B responses. In the dark, both phy A and phy B are There are many published papers regarding GAs’ func- distributed throughout the cytoplasm. When exposed to con- tions in higher plants (Shao et al., 2002). Nevertheless, the tinuous red light, nuclear translocation of phy A by 4.5 h, definite role of GAs in signaling and moreover their inter- whereas thanslocation of phy B to the nucleus reaches a actions with phytochrome signal transduction are somewhat maximum only after 6 h. Taken together the results to date unclear, to date the best known GA signaling mutant, spy suggest a close connection between CTK and phytochrome (spindly) has been isolated on the bases of its light green signaling. With the recent identification of the CTK receptor leaves, increasing internode length and spindly growth phe- in Arabidopsis and the concerted effort inidentifying more notype, which is reminiscent of wild type plants after repeated CTK-specific genes, additional CTK-mediated interactions GA3 applications [1]. This spy phenotype also resembles the between light and CTK with undoubtedly surface [36]. phy B mutant phenotype. SPY has been cloned and encodes a TRP repeat protein with sequence homology to a serine- 4.3. ABA O-linked N-acetylglucoramine transferase and SPY is most likely a reprint of the GA response [1]. Other researchers ABA plays important roles in the transduction of signals isolated a recessive suppressor of the GA deficiency. This between higher plants and environment, in particular condi- disrupted gene is named RGA (repressor of bas-3) and the tion stresses, which is quite familiar to us [22,36]. One of RGA locus encode a member of the GRAS (VHIID) protein the most common stresses, UV-B radiation, acts on higher family, which includes SCR and GAI. RGA is demonstrated plants by the interactions between the phytochrome signal to localize to the nucleus of higher plant cells. Additionally, system and ABA signal transduction pathways, during which PATI, which is a remember of the GRAS (VHIID) protein higher plants reduce to the lowest extent of damage by adjust- family involved in phy A signaling, has been islated (Bolle ing their physiological and chemical reactions to the outside et al., 2000) implying the GRAS protein family may have a [26,27,34]. What is the most important advance in this aspect global role in high plant signal transduction. All members of is ABA signaling and RNA processing relationship in qus- the GRAS family also harbour structural motifs suggestive tion. It is clear that RNA processing is a critical feature of post of protein–protein interactions, which clearly indicate that transcriptional gene expression in all eucaryotes. Because the different pathways may intercept at the level of common inter- majority of genes (more that 80 of higher plant genes) contain acting variety as a part of a signal network [22,24,36,38–41] introns, tremendous diversity at the level of the proteosome. (Shao et al., 2002). Evidence is accumulating that early splicing plays an criti- Recent results have displayed more directly that phy- cal role in the regulation of ABA signaling, which is sure to tochrome and GAs are more closely interlined. For example, become a hot topic in plant molecular biology research in the the genes GA4 and GA4A, both encoding GA 3-hydroxylase. coming future. In fact, phy B promotes seed germination by increasing GA Schrocder (University of California, San Diego) and col- biosynthesis. Interestingly, GH4 but not GA4A is induced in a leagues isolated a new recessive ABA-hyper sensitive mutant, phy B-deficient mutant, indicating that the induction of differ- ABHI which shows ABA hypersensitive inhibition of seed ent GA hydroxylases showed that a functional GA signaling germination, ABA hypersensitive increases in cytosolic cal- system is necessary for the elongated hypocotyl phenotype cium in guard cells, stomatal closure and reduced wilting observed in phytochrome mutants. Gerdreau et al. (1999) L.-Y. Chu et al. / Colloids and Surfaces B: Biointerfaces 45 (2005) 154–161 159 also displayed that endoreduplication levels in Arabidop- short. Evidence also shows that a number of signaling inter- sis hypocotyls are under negative control of phytochrome, mediates interact directly with phytochrome, suggesting that whereas GAs have a positive effect on the endoreduplication. phytochrome may act as a nuclear workplace, forming protein GAs also affect flowering in higher plants, but in contrast to complexes that execute appropriate signaling subpathways phy B-induced delay in flowering, with an enhancing action by physical contact to other nuclear proteins. Certainly, there on flowering [36]. However, phy B does of course also mod- are also a number of phytochrome signaling intermediates ulate flowering through a GA-independent pathway. At this that are localized to the nucleus that do not interact with phy- point in time the interaction between phytochrome and GA tochrome directly (Ballerteros et al., 2001). signaling is somewhat hard to be explained. However, it is A general picture of phytochrome signaling transduction clear that phytochrome and GA signaling pathway do interact in higher plants in most cases is clear, just through which in order for higher plants to control such diverse developmen- higher plants sense the outside environment and make corre- tal processes as seed germination and flowering [40] (Shao sponding responses in gene expression and further physiolog- et al., 2002). ical, biochemical and individual levels to reduce the damage brought about by environmental stresses. We firmly believe 4.5. Ethylene in the fact that reasonable integration of different updated information from diversified disciplines, in particular ones of In the dark ethylene inhibits hypocotyl elongation whilst life sciences, during the 21st century plays the most impor- in light ethylene promotes hypocotyl elongation. The cloning tant function in resolving the great dilemma (Population- and characterization of the Aarabidopsis flower gene has Resource-Ecoenvironment-Development) in relation to shown that it promotes cell elongation specific genes in the sustainable development confronted with humans [38–41]. apical hook region [26,27]. Interestingly, HLSI is thought Life sciences, especially molecular biology, is the basis to control this elongation by regulating either the transport for the resolutions. There are many problems remained or chemical modification of auxin. Moreover, auxin resistant to be investigated in forms of higher plant phytochrome mutants are ethylene insensitive. These results suggest that a signaling transduction. How is the nuclear signaling network three-way interconnected pathway between light and auxin controlled? One possible elegant way of controlling the be ethylene signaling [24]. By contrast to GAs, ethylene has signaling responses is at the level of nuclear translocation a positive effect on endoreduplication events in the hypocotyl [1,38,39,41,42] (Shao et al., 2002). How are constitutively in the light and in the dark (Gendreau et al., 1999). Although nuclear proteins controlled? One mechanism clearly involves the ethylene signal transduction pathway is relatively clear the 26s proteasome where by signaling components are there is still a long way to go before we fully understand the specifically targeted for degradation providing yet another integration of ethylene and phytochrome signaling in higher elegant way of controlling the signal flux. Additionally, the plants. protease may also be involved in phy A degradation itself. Why do only some phytochromes in higher plants show light dependent peculiar translocation? Why do some nuclear 5. Concluding remarks and future development components from speckles in the nucleus whilst others do not send? Why also the speckles different among various The recent progress in phytochrome research of higher classes of proteins? plants has been tremendous and at times it is hard to recon- Are most bona fide phytochrome signaling cascades cile and integrate all the incoming data into an overall picture. of higher plants short and nuclearly localized and is the The notion that phytochrome signal transduction represents cytoplasm merely a peripheral supporting component? How a linear chain of events is now outdated and it is increas- are the feedback signals traduced from the chloroplast to ingly clear that phytochrome signaling should be referred to the nucleus and what is the accurate mode of chloroplast as a multidimensional network [1]. In this paper, the authors in terms of photomorphological responses? What is the have attempted to introduce this complex network in terms relationship among the phytochrome signaling transduc- of molecular biology and cell biology, meanwhile shedding tion and different phytohormone signaling transduction light on recent and exciting findings with particular emphasis circuits in higher plants? How many common components on the role of the different subcellular compartments in con- (intermediates, sensors, adaptors, receptors, regulators, etc.) trolling phytochrome signaling cascades by trying to obtain have been shared between the two classes of important a deeper understanding from the angle of eco-environment. substances of higher plants? What is the most important, is One emerging topic in phytochrome signaling is undoubtedly that: how to make the best use of the data available from the that a wealth of signaling activities take place in the nucleus viewpoints of individual, community and eco-environmental frontier and the demonstration that phy A and phy B translo- levels to serve people, who are facing the vast surviving cate to the nucleus in response to light and that photoactive challenge? phytochrome can interact with nuclear DNA-binding pro- It is completely obvious that each cellular organelle has teins to regulate gene expression, demonstrate that at least its own specific role in terms of phytochrome signaling trans- some branches of phytochrome signaling are exceedingly duction. It is also clear that these multiple organelles are 160 L.-Y. Chu et al. / Colloids and Surfaces B: Biointerfaces 45 (2005) 154–161 interconnected in order to execute the appropriate cellular [14] R. Rizhsky, H.J. Liang, R. Mittlre, The combined effect of drought and physiological responses. Moreover, the extensive subcel- stress and heat shock on gene expression in tobacco, Plant Physiol. lular network of interactions and intersection between light 130 (2002) 1143–1151. [15] B. Mueller-Roebuck, C. Pical, Inositol phospholipid metabolism signaling and other signaling pathways are very impressive in Arabidopsis. Characterized and putative isoforms of inositol and complicated. How the numerous signals and pathways phospholipid kinase and Phosphoinositide-specific phospholipase C., are co-ordinated among cellular organelles and how this net- Plant Physiol. 130 (2002) 22–46. work is finely tuned in response to the change, in the light [16] Q. Gao, P. Zhao, X. Zeng, X. Gai, W. Sheen, A model of stomatal environment remain exciting future task. No doubt, the grow- conductance to quantify the relationship between leaf transpiration microclimate and soil water stress, Plant Cell Environ. 25 (2002) ing availability of functional genomics resources for isolating 1373–1388. mutations in genes of interest, advances in proteomics and the [17] R.B. Darnell, RNA logic in time and space, Cell 110 (2002) increasing feasibility of spectroscopy-based protein identifi- 545–550. cation and utilization of mass microarrays will make this field, [18] J. Leon, E. Raja, J.J. Sanchez, Wound signaling in plants, J Exp. one of the frontiers in molecular biology, the most exciting Bot. 52 (354) (2001) 1–9. [19] S. Dharmasiri, M. Estelle, The role of regulated protein degradation and prosperous and brightest focus! in auxin response, Plant Mol. Biol. 49 (2002) 401–409. [20] G. Hagen, T. Guilfoyle, Auxin-responsive gene expression: genes, promoters and regulatory factors, Plant Mol. Biol. 49 (2002) Acknowledgements 373–385. [21] A. DeLong, Mockaifisk, S. Christensen, Protein phosphorylatino in This work is jointly supported by National Key Basic the delivery of and response to auxin signals, Plant Mol. Biol. 49 Research Development Programe (G2000018605), Major (2002) 285–303. [22] L.M. Xiong, K.S. Stomacher, F.K. Hi, Cell singling during cod, Research Plan of NSFC (90102012), and Youth Scientific drought, and calf saffron, Plant Cell (Suppl.) (2002) S156– and Technological Foundation, Doctoral Initiation Founda- S183. tion of Chonqing University of Posts & Telecommunications [23] L.M. Xiong, F.K. Zhu, Abiotic stress signal transduction in plants: and Shao MA-Innovation Group Program Project of North- molecular and genetic perspectives, Physiol. Plant 112 (2001) west Sci-tech University of Agriculture and Forestry. 152–166. [24] J.K. Zhu, Plant salt tolerance, Trends Plant Sci 6 (2001) 66–71. [25] N.A. Eckanlt, Plant reproduction: insignts into the Abominable Mys- tery, Plant Cell 14 (2002) 1669–1673. References [26] N.A. Eckardt, Specificity and cross-talk in plant signal transduction: January 2002 Keystone Symposium, Plant Cell (Suppl.) (2002) [1] S.J. Moller, P.J. Ingles, G.C. Whitelam, The cell biology of phy- s9–s14. tochrome signaling, New Phytol. 154 (2002) 553–590. [27] N.A. Eckardt, Alternative splicing and the control of flower time, [2] W.S. Jia, Y. Xing, C.M. Lu, J.H. Zhang, Signal transduction from Plant Cell 14 (2002) 743–747. water stress perception to ABA accumulation, Acta Bot. Sin. 44 (10) [28] Y.M. Guo, S.H. Shen, Y.X. Jing, T.Y. Kuang, Plant proteomics (2002) 1135–1141. in the post-genomic era, Acta Bot. Sin. 44 (6) (2002) 6314– [3] M.B. Bonitott, M.E. Griffith, Cross-talk between cell division cycle 6341. and development in plants, Plant Cell 14 (2002) 11–16. [29] W. Yue, J. Wang, Q.L. Huang, W.J. Zheng, Z.C. Hua, Synergistic [4] A. Trewavas, Plant cell signal transduction: the emerging phenotype, activation of eukaryotic gene transcription by multiple upstream sites, Plant Cell (Suppl.) (2002) S3–S4. Prog. Biochem. Biophys. 29 (4) (2002) 510–513. [5] B.B. Jordan, Molecular response of plant cells to UV-B stress, Func. [30] Y.X. Tang, S.G. Liu, Cloning and expression of the, AtGRPq gene Plant Cell 29 (2002) 909–916. related to salt stress tolerence in Arabidopsis, Acta Biochim. Bio- [6] J. Flexas, H. Medrano, Energy dissipation in C3 plants under phys. Sin. 34 (6) (2003) 737–742. droughf, Func. Plant Biol. 29 (2002) 1209–1215. [31] G.H. Mao, Y. Guo, S.J. Chui, Wounding signals and signal [7] R. Swamp, G. Parry, N. Graham, T. Allen, M. Bennett, Auxin cross- transduction, Acta Boreal-Occident Sin. 22 (6) (2002) 1504– talk: integration of signaling pathways to control plant development, 1511. Plant Mol. Bol. 49 (2002) 411–426. [32] Q.J. Yu, Q. Wu, Z.P. Lin, J.F. Li, Advances of plant aquaporins [8] S.Y. Kwon, Y.J. Jeong, H.S. Lee, J.S. Kim, K.Y. Cho, R.D. Allen, research, Acta Scientiarum Naturalium Universitatis Pekinensis 38 S.S. Kwak, Enhanced tolerance of transgenic tobacco plants express- (6) (2002) 855–866. ing both superoxide dismutase and ascorbate peroxidase in chloro- [33] Z.S. Liang, F.S. Zhang, M.A. Shao, J.H. Zhang, The relations of plasts against methyl viologen-mediated oxidative stress, Plant Cell stomatal conductance, water consumption, growth rate to leaf water Environ. 25 (2002) 873–882. potential during soil drying and reweting cycle of wheat (Triticum [9] A. Mouradov, F. Cremer, G. Coupland, Control of flowering time: aestivum L.), Bot. Bull Acad. Sin. 43 (2002) 187–192. interacting pathways as a basis for diversity, Plant Cell (Suppl.) [34] Z.B. Zhang, P. Xu, J.H. Zhang, J. Wang, Advance on study of molec- (2002) S111–S130. ular marker and gene cloning and transgenes in drought resistance [10] G. Zotz, Arsenic and old plants, New Phytologist 156 (2002) 1–8. and water saving in crops, Acta Bot. Boreal-Occident Sin. 22 (6) [11] M.F. Mete, J.V. Winded, M. Matzke, A.J.M. Mattock, Short RNAs (2002) 1537–1544. can identify new candidate transposable element families in Ara- [35] H.B. Shao, H.M. Liang, The pre-treatment of Barley seeds affects bidopsis, Plant Physiol. 130 (2002) 6–9. on Regulation and control of the explant characters and discussion [12] H. Porta, M. Rocha-sosa, Plant lipoxygenases. Physiological and about their mechanism(I), Guihaia 21 (4) (2001) 347–352. molecular features, Plant Physiol. 130 (2002) 15–21. [36] H.B. Shao, The control of flowering time and photoreceptors in [13] R.O. Teskey, M.A. Mcguire, Carbon dioxide transport in xylem higher plants(I), Life Sci. Res. 5 (3) (2001) 149–152. causes errors in estimation of rates of respiration in stems and [37] H.B. Shao, The gene expression and control of flowering time in branchs of trees, Plant Cell Environ. 25 (2002) 1571–1577. higher plants, Biol. Biotech. 6 (2001) 12–18. L.-Y. Chu et al. / Colloids and Surfaces B: Biointerfaces 45 (2005) 154–161 161

[38] H.B. Shao, Z.S. Liang, M.A. Shao, Plant Molecular Biology in [41] H.B. Shao, Z.S. Liang, M.A. Shao, Adaptation of higher plant to China: opportunities and challenges, Plant Mol. Biol. Rep. (2005). stress environment and stress signal transduction, Acta Ecol. Sin. 25 [39] H.B. Shao, Z.S. Liang, M.A. Shao, Some changes regarding pho- (7) (2005) 1772–1781. tochemistry and molecular biology for 10 wheat genotypes at soil [42] H.B. Shao, Z.S. Liang, M.A. Shao, Investigation on dynamic changes water deﬁcits, Plant Soil (2005). of photosynthetic characteristics of 10 wheat (Triticum aestivum L.) [40] H.B. Shao, Z.S. Liang, M.A. Shao, Roles of ABA signal transduc- genotypes during two vegetative-growth stages at water deﬁcits, Col- tion during higher plant seed germination and maturation, Forestry loids Surf. B: Biointerf. 43 (1) (2005) 221–227. Studies China 5 (4) (2003) 29–38.