Photosynthesis Research 44: 183-190, 1995. © 1995 KluwerAcademic Publishers. Printed in the Netherlands.

Regular paper

Light-induced biogenesis of the light-harvesting complexes of Photosystems I and II Gene expression and protein accumulation

D a r y l T. M o r i s h i g e 1 & S u s a n n e Preiss

Department of Biology, Universityof California~LosAngeles, Los Angeles, CA 90024-1606, USA; 1Current address: Department of Biochemistry & Biophysics, TexasA&M University, College Station, TX 77843-2128, USA Received20 November1994;acceptedin revisedform21 January 1995

Key words: chloroplast, phytochrome, cab gene, pigment-protein, LHC

Abstract

The light-harvesting complexes of Photosystems I and II contain multiple chlorophyll-carotenoid-binding proteins. The stoichiometry and topology of the LHCs is precisely defined to optimally funnel captured light energy to the reaction center. The manner in which this exact arrangement is accomplished is not known. As an initial means to understand the mechanisms involved in establishing a functional LHC, the influence of light on LHC gene expression and protein accumulation was studied during the light-induced greening of etiolated wild type and chlorophyll b-less mutant barley seedlings. Light, involving phytochrome, promotes the expression of all LHC genes with the same relative kinetics. LHC protein accumulation closely parallels the increases observed in transcript levels. Differential accumulation of LHC transcripts or protein was not evident in wild type seedlings. Post-translational factors are likely to be involved in fine tuning the position and stoichiometry of the individual LHCs around the reaction center.

Abbreviations: CC - core complex; LHC - light-harvesting complex Introduction

Photosynthetic capability is preceded by many morphological changes that take place in a developing leaf, including the formation of chloroplasts from immature proplastids. Expression of both nuclear and plastid localized genes is required to provide the proteins that make up the photosynthetic apparatus (reviewed in Mullet 1988). Concomitant with chloroplast biogenesis is the synthesis and accumulation of different LHC proteins. The LHC genes are located in the nucleus as small multigene families (reviewed in Green et al. 1991; Jansson 1994). The proteins are synthesized as precursor proteins in the cytoplasm with N-terminal transit sequences. Upon import into the plastid the transit sequence is cleaved, the LHC protein binds chloro-

phylls and xanthophylls and is inserted into the thylakoid membrane, where it assembles with its respective CC (reviewed in Chitnis and Thornber 1988). The exact order of these events is not known. At least four distinct LHC II components have been identified, each involved in energy transduction to the PS II reaction center (reviewed in Thornber et al. 1991). LHC IIb is the major LHC II component, binding approximately 43% of the total chlorophyll. In the thylakoid membrane this complex exists as a trimer, containing at least three apoproteins of 25-29 kD (Peter and Thornber 1991). The genes coding for the LHC IIb apoproteins (Lhcbl,2,3) have been isolated from many species and their expression has been well characterized (Chitnis and Thornber 1988; White et al. 1992). LHC IIb gene expression is regulated in

184 part by phytochrome (Silverthorne and Tobin 1984). At least three other LHC II components LHC IIa, LHC IIc and LHC IId (coded by the Lhcb4, Lhcb5 and Lhcb6 genes, respectively) are associated with PS II. LHC IIa contains a single apoprotein of 31 kD in barley (Peter and Thornber 1991; Morishige and Thornber 1992) or 29 kD in spinach and pea (Camm and Green 1980; Bassi et al. 1987; Peter and Thornber 1991). LHC IIc contains a major apoprotein of 28 kD (Dunahay et al. 1987; Bassi et al. 1987; Peter and Thornber 1991). LHC IId contains a single protein of 21 kD (Dunahay and Staehelin 1986; Bassi et al. 1987; Peter and Thornber 1991). Together, these minor LHC components bind about 10% of the total chlorophyll along with varying amounts of the xanthophylls lutein, neoxanthin and violaxanthin (Peter and Thornber 1991; Bassi et al. 1993). Three pigmented LHC I sub-complexes have been identified in PS I, binding about 20% of the total chlorophyll (Thornber et al. 1991). LHC Ia (LHC 1-680,) contains two proteins of 24 and 21.5 kD, the Lhca3 and Lhca2 gene products, respectively (Ikeuchi et al. 1991; Knoetzel et al. 1992; Welty and Thornber 1992). Two similar yet distinct proteins of 21 and 20 kD, coded by the Lhcal andLhca4 genes, are associated with LHC Ib (LHC 1-730; Ikeuchi et al. 1991; Knoetzel et al. 1992; Welty and Thornber 1992; Anandan et al. 1993). LHC Ib can be isolated as an oligomer, probably a trimer, by sucrose gradient centrifugation or non-dissociating Deriphat-PAGE (Knoetzel et al. 1992; Preiss et al. 1993). LHC Ic contains a single protein of 17 kD. Nterminal sequencing has identified the protein as the psaF gene product (Anandan et al. 1989). The major LHC I components, LHC Ia and LHC Ib, bind chlorophylls a and b and the xanthophylls violaxanthin and lutein (Thornber et al. 1993). In contrast, LHC Ic primarily binds chlorophyll a, with only small amounts of chlorophyll b and xanthophylls associated with the complex (Preiss et al. 1993). Analysis of the primary structures of LHC I and II proteins reveals a strikingly high degree of similarity among them (reviewed in Green et al. 1991; Jansson 1994). Early structural models of the LHC lib protein predicted the presence of three membrane spanning regions with the amino terminus of the protein exposed to the chloroplast stroma and the carboxy-terminus in the thylakoid lumen (Karlin-Neumann et al. 1985). Electron diffraction analysis of two-dimensional crystals of LHC IIb confirmed this general model and has provided insights into the arrangement of the LHC IIb protein and its associated pigment co-factors at atomic

resolution (Ktihlbrandt et al. 1994). Due to the high amino acid sequence similarity between LHC lib and the remaining LHC proteins, it is highly probable that the other LHCs are oriented in the thylakoid membrane in a similar manner. With each LHC presumably possessing the same relative three-dimensional structure, the factors involved in the assembly of the LHCs into highly ordered structures remain to be elucidated. LHC I and LHC II components must not only assemble with their respective CC, but the orientation and stoichiometry of each LHC with respect to the other LHCs in a photosystem are also important. Knowledge of the expression patterns of all the LHC genes and how they relate to the accumulation of the proteins they encode would aid in the elucidation of the controls involved in the assembly of the photosynthetic apparatus. Presently, we have used identified LHC II genes from barley to study the involvement of phytochrome in their gene expression and the patterns of light-induced transcript accumulation in developing barley chloroplasts. In addition, LHC protein accumulation is followed during chloroplast biogenesis.

Materials and methods

Barley seeds (Hordeum vulgare cv. Prato) were imbibed in distilled water overnight and allowed to germinate for 5 d in complete darkness before light treatments. For phytochrome studies, etiolated seedlings were exposed to red light (10/iE/m2/s) for 2 min and/or far-red light (33.6/zE/m2/sec) for 10 min immediately following the red light treatments. Seedlings were returned to complete darkness for an additional 6 h before the tissue was prepared for total RNA isolation. For biogenesis studies, 5-day-old etiolated seedlings were placed under fluorescent light supplemented by tungsten lighting (80 #E/m2/sec) for zero to 36 h. Control plants were grown in a greenhouse under natural light conditions or in a light-tight dark growth chamber before harvesting. A partial-length cDNA clone for LHC IIc (Lhcb5) with high sequence similarity to previously identified Lhcb5 genes (Pichersky et al. 1991; S~rensen et al. 1992) and covering approximately 80% of the full-length message was isolated from a lambda gtl 1 library. A full-length cDNA of LHC IIa (Lhcb4; Morishige and Thornber 1992), a full-length genomic LHC lib clone (Lhcbl; Chitnis et al. 1988) and a partiallength LHC Ib cDNA clone (Lhcal; Anandan et al. 1993) were also used as probes.

185

Fig. 1. Phytochrome control over steady-state RNA levels for LHC Ila, LHC IIb and LHC lIc. Etiolated barley seedlings (E) were exposed to either red (R), red followedby far..red (R/FR) or far red (FR) light. Total RNA was isolated six hours after light treatments. RNA was also isolated from seedlings exposed to 6 h contim~ous light (6 h) or grown under normal day-night conditions (M). Each lane contains 4/zg total RNA.

Fig. 2. Phytochrome control over steady-state RNA levels for Lhcal and Lhcb4 genes encoding the 21 kDa LHC Ib end the 31 kDa LHC IIa (CP29) apoproteins in the chlorina f2 barley mutant. Total RNA isolated from five day-oldetiolated chlorina f2 seedlings

treated with the same light regimes as described in Fig. 1 was used.

Total RNA was isolated according to Flores and Tobin (1987) from fully-expanded areas of primary leaves above the sheath of 5-6-day-old barley seedlings after the different light treatments. Equal amounts of total RNA (4 #g) from different light treatments were separated on 1.2% agarose gels and blotted to Nytran membranes (Schleicher and Schuell). Hybridizations were carried out according to standard protocols (Ausubel et al. 1990). Probes were labeled by random priming and used for hybridization at a probe concentration of 2.5 x 106 cprn/ml. Highest stringency washes were at 60 °C in 0.1 x SSC (1 x SSC: 150 mM NaC1, 15 mM Na3C6H5OT.H20) and 0.5% SDS. For analysis of protein, fully-expanded sections of whole leaf tissue from seedlings treated with different light regimes were ground in liquid nitrogen. Total protein was extracted b y incubating the ground tissue in SDS-PAGE sample buffer (10 mM Tris, pH 6.8, 2%

Fig. 3. RNA gel blot analysis of the accumulationof LHC message during biogenesis of etiolated barley seedlings. Total RNA was harvested from etiolated seedlings (E), seedlings exposedto 0.5-24 h of continuous light and from seedlings grown under natural day-night conditions (M). Each lane contains 4/~g total RNA.

SDS, 2% ¢3-mercaptoethanol, 2% glycerol; 100 mg tissue to 100 ~tl extraction buffer) at 75 °C for 30 min. L,~u'ge debris were separated from the extracts by brief centrifugation. Equal volumes of protein extracts from e~tch time point (typically 25 #i) were loaded directly onto fully-denaturing SDS gels (Peter and Thornber 1991). Following electrophoresis proteins were transferred to nitrocellulose and probed with LHC specific antibodies MLH9 and MLH 12 (a kind gift of Dr Sylvia Darr; Darr et al. 1986).

Results Phytochrome control over L H C gene expression

Phytochrome plays a crucial role in the expression of the LHC IIb genes, apparently at the level of transcription initiation (Silverthorne and Tobin 1984) by a partially understood signal transduction pathway (Chory 1993). To determine if phytochrome plays a similar role in the expression of other LHC II genes, message accumulation for LHC IIa and LHC IIc was studied in etiolated barley seedlings exposed to red light. Fiveday-old etiolated barley seedlings, exposed to a 2 min pulse of red light followed by an additional 6 h of total darkness, exhibit a large accumulation of each of the LHC II messages, when compared to levels from etio-

186 lated seedlings (Fig. 1). Transcript levels per gram tissue are about equal to those from seedlings exposed to 6 h of continuous illumination. An increased accumulation of LHC message is not observed when plants are immediately exposed to 10 min of far-red light after the 2 min red light pulse (Fig. 1). Similarly, message levels remain relatively low when seedlings are only exposed to far-red light. Under all light regimes, the accumulation of message for LHC IIa and LHC IIc closely parallels the accumulation of LHC IIb transcripts (Fig. 1). Cross-hybridization between the different probes was not observable under the hybridization and washing conditions used in this study (data not shown). Although only the steady-state transcript levels from the various LHC II genes are being observed in these experiments, the accumulation of transcripts for the minor LHC IIs is apparently under the control of phytochrome, most probably at the level of transcription, as has been clearly shown for LHC IIb (Silverthorne and Tobin 1984). An early study on the chlorina-f2 chl b-less mutant of barley demonstrated that light initiated the accumulation ofLHC IIb message in the mutant similar to wild type plants (Apel and Kloppstech 1978). In contrast, LHC IIb protein was not present in the thylakoid membrane of mutant plants, indicating that control over protein accumulation was a post-transcriptional event. At the time, genes or even knowledge of the multiple apoproteins for other LHC components were not available. To extend this early study, we investigated the phytochrome control over message accumulation for the genes of LHC Ib and LHC IIa (Lhca 1 and Lhcb4, respectively) in the chl b-less mutant. Expression of the Lhcal and Lhcb4 genes in the mutant (Fig. 2) closely parallels expression patterns in wild type tissue (Fig. 1; Anandan et al. 1993), indicating that each gene has a similar response to phytochrome in both mutant and wild type.

Accumulation of LHC mRNA and protein during chloroplast biogenesis During the light-triggered development of a chloroplast from an etioplast, many nuclear-coded proteins are transported into the chloroplast, where they assemble with chloroplast-coded proteins to form multisubunit complexes. As a means to understand the mechanism that controls the assembly and positioning of the LHC IIs, transcript accumulation for three different LHC II proteins was studied during the lightinduced biogenesis of an etioplast into a chloroplast.

Five-day-old etiolated barley seedlings were exposed to continuous light for up to 24 h and total RNA was isolated from primary leaves at various times. RNA gel blots containing equal amounts of total RNA from tissue samples taken at different developmental time points were probed with the LHC II genes (Fig. 3). Equal loadings per lane were verified by observation of the intensity of ethidium bromide-stained rRNA bands on the gels (data not shown). In each case LHC message accumulation was readily apparent after seedlings were exposed to two hours of constant illumination with little or no message detectable prior to this time point. Maximal levels of transcript were evident by 8 h of light exposure after which the levels remained relatively constant up to the 24 h time point (Fig. 3). The accumulation of LHC II proteins was then correlated to LHC II transcript levels. Total protein was isolated from primary leaves of seedlings exposed to different lengths of continuous illumination. Samples were loaded on SDS-gels on the basis of equal volumes of protein extract per gram fresh weight of tissue. Total protein gels of proteins extracted from tissue treated with different light regimes stained with Coomassie blue showed little variation in staining intensity (data not shown). Antibodies reacting with the LHC proteins were used to probe blots of the total protein extracts separated by SDS-PAGE. Monoclonal antibodies (Darr et al. 1986) that react with at least three different LHC IIb proteins (MLH9) or with all of the LHC I and LHC II proteins except for those ofLHC IIb (MLH12) were used in this study. The LHC IIb proteins were evident in total protein extracts after 4 h exposure to continuous light (Fig. 4, lower panel). Maximal levels of LHC IIb protein are evident in samples from seedlings exposed to 18 h of light and remain at this level up to 36 h. Similarly, using the antibody MLH12, that reacts with LHC I (LHC Ia and LHC Ib) and LHC IIs (LHC IIa, LHC IIc and LHC IId), it is apparent that these components accumulate with the same relative kinetics as LHC IIb. Each protein initially appears after 4 h of continuous light exposure and reach maximal levels after 18 h exposure to continuous light (Fig. 4, upper panel).

Discussion

A fundamental problem remaining to be investigated in chloroplast biogenesis is exactly how a photosystem with a defined complement of similar yet distinct LHCs is assembled into the highly ordered structure

187

Fig. 4. LHC proteinaccumulationdtwingthe biogenesisof etiolatedbarleyseedlings. The upperpanel followsthe accumulationof LHC protein except LHC IIb. The lower panel follows the accumulationof LHC lib proteins. Total protein from equal amounts of fresh tissue originating frometiolated seedlings (E) exposedto increasing lengthsof continuous illumination (0.5-36 h) were separatedby SDS-PAGEand transferred to nitrocellulose. Blots were probedwith LHC specificantibodies.

found in the thylakoid membrane. Presently, there is not an unequivocal model for the relative positioning of the different LHC II subunits in PS II, although current models place the minor LHCs close to the CC with the LHC IIb components on the periphery (Morrisey et al. 1989; Peter and Thornber 1991; Bassi and Dainese 1992; Harrison and Melis 1992). Uncertainty remains regarding the identification of LHC II subunits that contact specific CC II subunits, and whether LHC II is organized into one large or several smaller complexes that each interact with CC II. Subcomplexes containing specific LHC IIs have been isolated and emphasize the highly ordered arrangement of the individual LHCs with respect to the CC and each other (Peter and Thornber 1991; Bassi and Dainese 1992). Two possible mechanisms can be envisaged to initiate the ordered assembly of the minor LHCs followed by LHC IIb around the core complex during chloroplast development: 1) When seedlings are exposed to light, the genes for the minor LHC IIs are expressed first, the proteins are transported into the chloroplasts where they assemble with their cofactors and with the core complex. The LHC IIb genes are expressed later and their proteins assemble around the pre-formed core of minor LHC II complexes; or 2) Upon exposure to light all LHC genes are expressed at the same time. Amino acid sequence motifs within the proteins or other factors are then employed to determine the exact

orientation of the LHC IIs around the core complex and between each other. Previous studies have shown that phytochrome plays an important role in the expression of several different LHC I and LHC II genes (White et al. 1992; Kellmann et al. 1993; Anandan et al. 1993). It is now clear that phytochrome is controlling Lhcb4 and Lhcb5 gene expression as well. LHC IIa, LHC IIb and LHC IIc message accumulation is apparent in etiolated barley seedlings exposed to red light (Fig. 1). This effect is reversible by exposure to far-red light immediately following the red light pulse. A similar response to phytochrome for the two LHC genes tested, Lhca 1 and Lhcb4, was observed in the chlorina f2 barley mutant (Figs. 1 and 2). These experiments show that the same signal transduction pathway that regulates the expression of the LHC IIb genes in both wild type and mutant seedlings is also regulating expression of the genes for the minor LHC IIs and the LHC I's. Transcripts for LHC IIa, b and c were equally detectable by RNA gel blot analysis after exposing etiolated seedlings to 2 h of continuous illumination (Fig. 3). Message levels for each LHC increased steadily with up to eight hours of illumination and remained relatively constant beyond this time point. Similar patterns of transcript accumulation during chloroplast biogenesis have been observed for LHC I genes (Anandan et al. 1993) and in the chlorina f2 chlorophyll b-less

188 barley mutant (Preiss and Thornber 1995). Together, these data indicate that while light contributes to the overall expression of LHC genes, the individual LHC genes are not differentially expressed during the early stages of greening. Thus, translational or posttranslational factors modulate the levels of the specific LHCs during assembly of a photosystem. The majority of LHC proteins are encoded by a very small number of genes. The LHC IIb genes comprise the largest family, consisting of up to 16 members in one species (reviewed in Jansson 1994). Our study does not address the possibility of differential gene expression for the genes in a specific family, as has been observed within the LHC IIb gene family (Sheen and Bogorad 1986; Karlin-Neumann et al. 1988; Piechulla et al. 1991; White et al. 1992). The functional significance of this expression pattern is not known, since type-specific LHC IIb proteins apparently accumulate with the same relative kinetics during greening (see below; Sigrist and Staehelin 1994). To further define the mechanism controlling LHC assembly, LHC protein accumulation was investigated during greening of etiolated barley seedlings using LHC specific antibodies. LHC protein was detectable in total leaf extracts after etiolated seedlings were exposed to four hours of continuous illumination. Protein levels increased equally up to about 18 h of illumination and then remained steady beyond this time point. Similar to the transcript levels, no detectable differences in LHC protein accumulation were observed. These data are consistent with other studies using different antibodies against either LHC IIb and LHC I proteins to trace the accumulation of the proteins during greening (Anandan et al. 1993; Sigrist and Staehelin 1994). In these studies the different LHCs were detected initially after about four hours of constant illumination. Furthermore, when type-specific antibodies were used against the three different LHC IIb proteins, no differences in the kinetics of protein accumulation were detected during greening (Sigrist and Staehelin 1994). This is especially compelling since during greening of etiolated chlorina-f2 barley seedlings, each LHC IIb protein is detectable by antibodies, although in fully-developed chlorina f2 tissue the smallest LHC lib component (25 kD Type III) is one of the major LHC IIs remaining with a notable abscence of the other two LHC IIb proteins (Harrison and Melis 1992; Harrison et al. 1993; Preiss and Thornber 1995). The changes in steady-state protein levels observed during greening likely reflect steady-state amounts of LHC subunits functionally assembled in the thylakoids and

not to excess pools of free LHC apoprotein. Since little chlorophyll exists in a free state in the thylakoid membrane, it is probably bound to the LHC proteins shortly after synthesis. Chlorophyll b synthesis closely parallels the accumulation of LHC IIb protein during early greening (Tanaka and Tsuji 1985; Shimada et al. 1990). The accumulation of LHC IIb closely correlates to the appearance of whole chain electron transport about four hours after illumination (Ohashi et al. 1989). Together, the observations that transcript and protein levels for all of the LHC proteins increase similarly in response to light strongly suggest that posttranslational factors participate in the coordination and assembly of the LHCs in defined stoichiometries around their respective photosystems. Sequence motifs in the proteins could contribute to the assembly and localization of the specific LHCs around each photosystem. All LHC proteins share regions of high sequence similarity and are closely related (reviewed in Green et al. 1991; Jansson 1994). Little evidence is available at this time to point to specific domains within the LHC proteins which direct the LHCs to specific locations. Sequence comparisons have identified short putative LHC I-specific domains (Schwartz et al. 1991). In the LHC IIa sequence a unique region of 42 amino acids is evident within one of the areas of high sequence similarity shared by all LHC II proteins (Morishige and Thornber 1992). The functional significance of these motifs remains to be elucidated. Pigments play a crucial role in LHC assembly. Studies with chl b-deficient (Greene et al. 1988; Knoetzel and Simpson 1991) and chl b-less (White and Green 1987; Harrison and Melis 1992; Peter and Thornber 1991; Preiss and Thornber 1995) mutants have demonstrated the importance of chl b in the stabilization of LHCs in the thylakoid membrane With these mutants a hierarchy of chlorophyll binding is observed in which LHCs proximally located to the CC are able to bind pigments and assemble with the CC at the expense of the more peripheral LHCs. In vitro reconstitution experiments have demonstrated that a full complement of pigments, including xanthophylls, are necessary and sufficient to form stable pigmented complexes similar to LHC monomers, additional factors are apparently not required (Plumley and Schmidt 1987; Paulsen et al. 1990). Pigments apparently induce folding of the LHC IIb protein in vitro into a tertiary structure closely resembling native LHC IIb (Paulsen et al. 1993). Furthermore, the final ratio of bound pigments in a reconstituted complex is independent of the ratio of pigments in the initial reconstitution mixture (Paulsen

189 et al. 1990), indicating that structural motifs in the LHC protein prescribe which pigments are to be bound to the protein. This process must be highly specific, since only the 25 kD Type III LHC IIb (Lhcb3) is found in the chl b-less barley mutant (Harrison and Melis 1992; Harrison et al. 1993; Preiss and Thornber 1995), despite the high amount of sequence similarity with the Type I and II LHC IIb (Lhcbl and Lhcb2) proteins. Studies of the biogenesis of the LHC complexes in barley seedlings grown under intermittent light also have demonstrated the importance of pigments in the assembly process. Pulse-chase experiments show that LHC IIb assembles first with pigments as a monomeric complex. Only after formation of pigmented monomers is the appearance of the oligomeric forms ofLHC IIb evident (Dreyfuss and Thornber 1994a). Similarly, during the early steps of greening the LHC I complexes are first observed as monomeric subunits, which later form higher order units and assemble with the CC (Dreyfuss and Thornber 1994b). These studies begin to define the steps of LHC assembly. Additional studies are required to further reveal the complex regulatory steps involved in the assembly of the photosynthetic apparatus.

Acknowledgements This work was supported by U.S. Department of Agriculture/Cooperative State Research Service Award No. 93-37306-9577 to J. Philip Thornber. DTM was supported in part by a University of California Systemwide Biotechnology Research and Education Program Fellowship and a University of California Dissertation Year Fellowship.

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Light-induced biogenesis of the light-harvesting complexes of Photosystems I and II : Gene expression and protein accumulation.

The light-harvesting complexes of Photosystems I and II contain multiple chlorophyll-carotenoid-binding proteins. The stoichiometry and topology of th...
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