JXB Advance Access originally published online on October 8, 2004
Journal of Experimental Botany 2004 55(408):2541-2548; doi:10.1093/jxb/erh273
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RESEARCH PAPER |
The early light-inducible protein (ELIP) gene is expressed during the chloroplast-to-chromoplast transition in ripening tomato fruit
Department of Biology, Smith College, Northampton, MA 01063, USA
* To whom correspondence should be addressed. Fax: +1 413 585 3786. E-mail: cwetzel{at}email.smith.edu
Received 25 March 2004; Accepted 11 August 2004
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Abstract |
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Chloroplast-to-chromoplast transitions during fruit ripening require massive transformation of the plastid internal membrane structure as the photosynthetic apparatus is disassembled. Early Light-Inducible Proteins (ELIPs) are known to accumulate in chloroplasts during thylakoid biogenesis and under stressful conditions. To determine if ELIP may also play a role in thylakoid disassembly during the chloroplast-to-chromoplast transition, ELIP mRNA expression was measured in tomato, Lycopersicon esculentum Mill. cv. Rutgers. An EST clone was identified in the Tomato Genome Project/Solanaceae Genomics Network database that has high sequence similarity with the amino acid sequence of Arabidopsis ELIP1 and ELIP2. It has complete identity in the two conserved regions of the protein. Genomic Southern blots indicate that the gene is a single copy in tomato. The genomic sequence shows the three-exon structure typical of ELIP sequences from other species. mRNA for this gene is barely detectable on northern blots from etiolated seedlings, but transiently accumulates to high levels 2 h after transfer to the light. Greenhouse-grown tomatoes were used to measure ELIP mRNA accumulation during fruit development and ripening. Tomato ELIP mRNA is detectable in all stages of fruit ripening, but is most abundant in the breaker/turning stage of development. A survey of tomato EST databases revealed that ELIP cDNA is also relatively abundant in developing flowers, which contain yellow chromoplasts. Combined, these results suggest that ELIP may play a newly-recognized role in the chloroplast-to-chromoplast transition process.
Key words: Chloroplast, chromoplast, early light-inducible protein, fruit ripening, thylakoid
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Fruit ripening is characterized by many physiological changes, including fruit softening, sugar accumulation, and the production of chemicals associated with aroma, colour, and taste. After major fruit expansion, specific signals trigger the final ripening process. In climacteric fruit ripening, light and ethylene are two of the signals that initiate the ‘breaker’ stage, the first visible indication of massive co-ordinated chloroplast-to-chromoplast conversion (Gillaspy et al., 1993
; Alexander and Grierson, 2002). Tomato (Lycopersicon esculentum) is a climacteric fruit with both ethylene-dependent and -independent pathways that regulate ripening-related gene expression (reviewed in Zegzouti et al., 1999; Giovannoni, 2001, 2004; Alexander and Grierson, 2002).
Chromoplasts are plastids that accumulate high amounts of coloured carotenoids in plastoglobuli, crystals, and/or internal membraneous systems. Tomato fruit chromoplasts accumulate lycopene in crystals and plastoglobuli (Bathgate et al., 1985; Price et al., 1993; Fraser et al., 1994) as a result of altered gene expression associated with carotenoid synthesis (reviewed in Bramley, 2002). During the controlled process of transition, photosynthesis ends, chlorophyll is degraded, thylakoids are disassembled, and a new internal organization is created (Thomson and Whately, 1980; Piechulla et al., 1987; Lawrence et al., 1993; reviewed in Price et al., 1993). Gene expression during this process can be categorized into genes that are constitutive, i.e. ripening-independent; genes that cause ripening to occur; and genes that are expressed in response to ripening signals and that are responsible for physiological changes.
Extensive research has helped identify many of the biochemical steps associated with carotenoid formation and the physiological state of the thylakoids during the chloroplast-to-chromoplast transition. The focus of this study is to determine whether a particular class of thylakoid proteins, the Early Light-Inducible Proteins (ELIPs), may be involved with the transition process.
ELIP was first identified in pea as a transiently expressed, chloroplast membrane-targeted product present at the earliest stages of greening after an etiolated-to-light transition (Kolanus et al., 1987; Meyer and Kloppstech, 1984). ELIPs have now been identified in the genomes of many plant species. Derived amino acid sequence and hydropathy plot comparisons revealed a striking structural homology between ELIPs and light-harvesting complex proteins (LHCs, encoded by Lhca/b genes) (Grimm et al., 1989; Jansson, 1999; Montané and Kloppstech, 2000). Hydropathy plots of ELIP sequences indicate that there are three putative membrane-associated helices in the mature protein. Within two of these hydrophobic regions, I and III, is a tridecapeptide motif that is homologous to motifs in hydrophobic regions I and III of LHCs. The presence of this motif raised the question of the evolutionary and functional relationship between ELIPs and LHCs (Grimm et al., 1989; Green et al., 1991; Jansson, 1994; Montané and Kloppstech, 2000). ELIPs are incorporated into the thylakoid membrane fraction of chloroplasts (Meyer and Kloppstech, 1984; Scharnhorst et al., 1985; Grimm and Kloppstech, 1987; Grimm et al., 1989; Cronshagen and Herzfeld, 1990; Adamska and Kloppstech, 1991; Braun et al., 1996) after plastid import and cleavage of a transit peptide, yielding mature proteins of 13–20 kDa, depending on the species. Binding of chlorophyll to purified ELIP has been demonstrated and is required for insertion of the protein into etioplast membranes (Adamska et al., 1999, 2001).
Pea, barley, and Arabidopsis ELIP mRNAs are expressed before Lhcb or RbcS messages, within 1–2 h after illumination of etiolated seedlings. Accumulation of the protein lags behind the peak mRNA abundance (Cronshagen and Herzfeld, 1990; Funk et al., 1995). Expression is also influenced by developmental stage; in the developmental gradient of a light-grown barley leaf, ELIP expression was greatest at the immature leaf base and undetectable in the mature leaf tip (Grimm et al., 1989; Montané et al., 1997). Its early expression upon illumination of etiolated seedlings and during chloroplast development led to the hypothesis that ELIPs play a role in plastid development, perhaps as a structural proxy for LHC that is replaced as a last step in photosystem assembly (reviewed in Adamska, 2001).
RNA hybridization, microarray, and cDNA analyses show that ELIP mRNA increases in abundance in response to a variety of stress-related signals. These include treatment with salt, heat, abscisic acid, cold, desiccation, aluminium, high CO2, and senescence (Montané et al., 1997; Król et al., 1999; Shimosaka et al., 1999; Adamska, 2001; Harari-Steinberg et al., 2001; Bhalerao et al., 2003; Binyamin et al., 2001; Provart et al., 2003). ELIP expression is also induced in mature plants by high light stress. Under these conditions, ELIP mRNA levels are only transiently elevated while protein levels remain elevated until the plant is returned to lower, prestress light intensities (Adamska et al., 1992, 1993; Potter and Kloppstech, 1993). Concurrent with ELIP protein accumulation, D1 protein in the photosystem II (PSII) reaction centre decreases in abundance and there is a decrease in PSII activity (as measured by chlorophyll variable fluorescence). During recovery of photosynthesis from photoinhibition, ELIP protein levels decrease. Degradation of ELIP is attributed to a thylakoid-associated, serine-type, ATP-independent protease that is activated under non-stress conditions (Adamska et al., 1996). A role for ELIP in resistance to drought stress is indicated by several studies. Expression of an ELIP-like gene in Craterostigma plantagineum, a plant that can survive and recover from extreme dryness, is influenced by abscisic acid and light levels and is induced by drought. Constitutive expression of the ELIP gene in Helianthus annuus confers drought tolerance (Alamillo and Bartels, 1996; Ouvrard et al., 1996). Two ELIP genes in gametophytes of the moss Tortula ruralis also undergo increases in expression in response to desiccation, salt, high light, and rehydration stress (Zheng et al., 2002).
The work presented here demonstrates that ELIP mRNA accumulates during the earliest stage of transition from chloroplast to chromoplast in tomato. This suggests a previously unrecognized function for ELIP in the conversion of chloroplasts to chromoplasts.
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Materials and methods |
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All sequencing was carried out by MWG Biotech (High Point, North Carolina). All PCR reactions were carried out in an Eppendorf Mastercycler Gradient machine. Lycopersicon esculentum Mill. cv. Rutgers and Arabidopsis thaliana L. ecotype Columbia were used for all analyses. DNA isolation was carried out using a DNeasy Plant Kit (Qiagen) and total RNA was isolated using the Purescript RNA Isolation kit (Gentra Systems).
Identification of tomato ELIP
A putative Lycopersicon esculentum ELIP cDNA sequence was identified in the Solanaceae Genomics Network database (SGN; http://www.sgn.cornell.edu/) by using the Arabidopsis ELIP sequences (At3g22840, At4g14690) in BLAST searches. 17 clones of a single gene were identified (data not shown), and one of the longest clones was chosen for further study (cLEN3H15; Genbank AW221686). The clone was obtained from the Clemson University Genomics Institute (http://www.genome.clemson.edu/) and the insert identity was verified by bidirectional sequencing. This sequencing information is more complete than the partial sequences reported for this clone in the SGN and Genbank databases.
Southern hybridization
Genomic DNA was isolated from tomato leaves and DNA quality was checked on ethidium-bromide-stained agarose gels (not shown). Approximately 7 µg of DNA was digested with EcoRI, SpeI, or BamHI at 37 °C for 6 h. Digested DNA was run on an agarose gel and blotted to nylon membrane (Immobilon NY+) according to the manufacturer's instructions.
The tomato ELIP probe was synthesized by PCR amplification of the cLEN3H15 plasmid using primer set 1 described below. The probe was labelled with 32P by random priming (TaKaRa) and hybridization was carried out under high stringency conditions using the MiracleHyb Hybridization protocol (Stratagene). Hybridization signal was detected using a Typhoon PhosphorImager (Molecular Dynamics) and ImageQuant software. The digital image was minimally processed to crop and improve contrast.
Determination of intron position and sequence
Sequence information from the cLEN3H15 cDNA clone was used to design primers for the amplification of intron sequences from tomato genomic DNA. The primers were: (set 1) left primer 5'- AATGACTTCCTTTGCCATGC-3' and right primer 5'-CATCAGCTTGAAATTGTTATTGA-3' for a product of 743 bp, and (set 2) left primer 5'-AATAGGTTCGCGATCTATAC-3' and right primer 5'- AGCTCCCTTAACATATTCAG-3' for a product of 650 bp. Amplification was carried out using Promega PCR Core System I, with a program of 5 min at 96 °C, 35 cycles of 15 s at 94 °C, 30 s at 45 °C, 2 min at 72 °C, followed by 4 min at 72 °C. PCR products were cloned into pGEM-T Easy (Promega) and sequenced.
Determination of the 5' end of the ELIP mRNA
5'-RACE (Ambion FirstChoice RLM-RACE Kit) was carried out using total RNA isolated from de-etiolating tomato seedlings after 4 h in high light. Two sets of gene-specific primers were used: inner1 5'-CGATGAAATTGGTGCTTGGT-3' and inner2 5'-CCGGACCACTGAATGAGAA-3'; and outer1 5'-AATGCACTTGACCCCAAGAA-3' and outer2 5'-ATGCACTTGACCCCAAGAA-3'. Four independent 5'-RACE products were cloned into pGEM-T Easy and sequenced; all contained the same 5' sequence information. The complete tomato ELIP gene sequence (combined results from EST sequencing, intron sequencing, and 5'-RACE) was deposited in Genbank (AY547273).
Plant growth and total RNA isolation
Seedlings: Tomato seeds were sown on standard seedling mix in small pots. The pots were left in the light at 22 °C for 24 h to promote germination and then moved into the dark at 22 °C for 10 additional days. For de-etiolation, seedlings were moved to the light (230 µmol m–2 s–1) for 0, 2, 4, 6, 8, and 12 h before cotyledon tissue was harvested and flash-frozen in liquid nitrogen. Total RNA was isolated and quality was checked on ethidium-bromide-stained formaldehyde gels (not shown). Replicate RNA samples were isolated from three separate seedlings for each time point.
Fruit: Tomato plants were grown in pots in the East Tennessee State University greenhouse (Johnson City, Tennessee, USA) under ambient light conditions during the winter and spring of 2002. Pollination of flowers was manually facilitated. Fruit were harvested and categorized based on size and colour. Total RNA was isolated from flash-frozen pericarp and quality was checked on ethidium-bromide-stained formaldehyde gels (not shown). Two replicate RNA samples were isolated from each of two separate sets of fruit (n=4).
RNA hybridization
Total RNA was run on a formaldehyde/agarose gel and blotted onto a nylon membrane (Immobilon-NY+, Millipore) according to the manufacturer's directions. Approximately 5 µg of total RNA was loaded per lane.
The tomato ELIP probe was synthesized as described above and hybridization was carried out under high stringency conditions. The hybridization signal was quantitated using the PhosphorImager and ImageQuant software. Blots were then reprobed with a tomato 18S rDNA probe by the same method. Sample-to-sample differences in total RNA loading were normalized according to the 18S rRNA signal. The cytoplasmic 18S rRNA signal was chosen to represent the relative amount of total RNA in each sample, thus the ELIP mRNA levels are measured compared with the pool of total RNA in the developing seedlings and fruits (Itai et al., 2003; Rao and Paran, 2003). Seedling mRNA blots were probed separately from fruit mRNA blots, so direct comparison of relative abundance between the two data sets is not possible.
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Results |
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Identification of the tomato ELIP sequence
Alignment of the predicted amino acid sequence of cLEN3H15 with that of characterized Arabidopsis ELIP sequences (Fig. 1) identifies the tomato EST as an ELIP gene product. There is 67% and 71%, respectively, overall amino acid similarity with ELIP1 and ELIP2 of Arabidopsis, and 100% identity in the conserved transmembrane regions I and III of the protein (Jansson, 1999
). Intron position is identical to that of the Arabidopsis genes, but exon nucleotide sequence similarity is much lower than that at the protein level (49% and 54% with At3g22840 and At4g14690, respectively) (data not shown; Genbank accession AY547273).
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Southern hybridization of genomic DNA with an ELIP probe indicated that it is a single copy gene in tomato (Fig. 2). Both BamHI and SpeI digestion resulted in a single hybridizing band. Double bands in the EcoRI lane are due to the presence of this restriction site within the ELIP probed sequence. Less stringent hybridization conditions did not reveal any other hybridizing bands in tomato DNA, but did permit hybridization to both Arabidopsis ELIP DNA sequences (not shown).
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Tomato ELIP mRNA increases in abundance during de-etiolation of seedlings
Northern blot hybridizations of total RNA isolated from de-etiolating seedlings after 0, 2, 4, 6, 8, or 12 h in the light were carried out to determine the temporal pattern of ELIP mRNA expression during the early stages of greening. As shown in Fig. 3, there is a marked, transient peak in abundance of ELIP mRNA at 2 h after transfer to the light relative to abundance at the other time points.
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Tomato ELIP mRNA increases in abundance during the breaker stage of fruit development
Northern blot hybridization of total RNA isolated from pericarp of fruits at different stages of development was carried out using the tomato ELIP probe. Figure 4 shows the fruit stages used (reviewed in Giovannoni, 2004
). There is a marked peak of abundance of ELIP mRNA in the breaker stage (5) of fruit development, compared with all the other stages (Fig. 5). ELIP mRNA was detectable in the immature green stages (1–3), but at a very low level. ELIP mRNA was detectable in the red (6) and over-ripe (7) stages, at a much lower relative level than in the breaker stage (5), but marginally higher than in the green fruit stages (1–4).
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Analysis of tomato ELIP EST abundance in a public database
The relative abundance of tomato ELIP EST clones represented in the Tomato Digital Expression Database (TDED; http://ted.bti.cornell.edu/digital/) was analysed in silico using TIGR LeGI TC116636 (ELIP) as a query. Representation of gene messages in EST collections has been used to crudely estimate expression levels (Jansson, 1999
). At a minimum, the presence of a specific EST indicates that its mRNA was present in the sampled tissue but the converse is not true (i.e. lack of EST may not indicate lack of mRNA). Table 1 presents the level of representation of EST clones for ELIP cDNA in each indicated plant tissue relative to the total number of ESTs collected for that tissue. A zero indicates that no ELIP cDNA was cloned from that tissue type. As shown in Table 1, there is more ELIP EST representation in tissues that are making or contain chromoplasts compared with non-chromoplast-containing tissues. Tomato flowers contain yellow chromoplasts, and ELIP EST clone abundance is high from mixed flowers (Table 1). Immature and mature green fruit have zero or relatively low ELIP EST clone abundance, but in the breaker stage the relative number of ELIP EST clones is higher (Table 1). The elevated ELIP EST representation continues in the red ripe stage. The stages present in the database may not exactly match the stages harvested in this study, but still provide a rough comparison with the northern blot data.
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Discussion |
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The results of this analysis of ELIP mRNA expression in ripening tomato fruit suggest that the protein may have a newly recognized role in the process of transformation of chloroplasts into chromoplasts. Much is known about the synthesis of carotenoids during this developmental process, but less is known about how the thylakoid is dismantled in a controlled way (Lawrence et al., 1997
). It is essential that the interior of the transforming plastid does not sustain significant photo-oxidative damage because the synthesis of carotenoids and continued function of the chromoplast requires extensive biochemical activity and reducing power (reviewed in Gillaspy et al., 1993; Aoki et al., 1998; Neuhaus and Emes, 2000).
ELIPs are proposed to have a photoprotective function in chloroplasts (reviewed in Adamska, 2001; Hutin et al., 2003). The precise role of the ELIP proteins in this process remains to be elucidated, however. While conversion to chromoplasts (transition) is in some ways similar to stressful (non-transition) conditions in chloroplasts, there are also fundamental differences. There is significant oxidative damage potential, and antioxidant components are up-regulated in plastids during the transition (Schantz et al., 1995; Aoki et al., 1998; Jimenez et al., 2002), similar to the situation in oxidatively-stressed chloroplasts. However, all of the stress-related responses described for non-transition chloroplasts share the feature of being short-term. When the stress abates, the chloroplast is programmed to return to its prestress state, if damage has been minimized, or to adjust to a post-stress state with a new level of photosynthetically functional thylakoids. If the stress exceeds the capacity of protective mechanisms then the plastid will bleach and lose photosynthetic function. It has been proposed that, in these situations, ELIPs may temporarily hold the photoactive chlorophyll molecules to prevent damage to D1, then help reassemble in the post-stress state (reviewed in Adamska, 2001); but see, however, Montané and Kloppstech (2000) for an argument against this hypothesis. Interestingly, in the green alga Dunaliella bardawil an ELIP homologous protein Cbr is up-regulated in response to stress at the same time that there is accumulation of the carotenoid beta-carotene and activation of the photoprotective xanthophyll cycle (Lers et al., 1991, 1993). There is evidence that Cbr binds zeaxanthin and that Cbr is degraded as violaxanthin is de-epoxidated to zeaxanthin (Levy et al., 1993), suggesting a function for Cbr in the xanthophyll cycle.
In chromoplast formation, in contrast to stressed chloroplasts, the transition is to an entirely new functional state that lacks chlorophyll and thylakoids. Many biochemical pathways are maintained in the mature chromoplast that are essential for fruit ripening. ELIP mRNA also increases in abundance during senescence of tobacco (Binyamin et al., 2001) and aspen leaves (Bhalerao et al., 2003), other situations of complete transformation of chloroplasts into a final non-green state, the gerontoplast. Chromoplasts and gerontoplasts differ somewhat in the degree of biochemical functions that they maintain, however, and thus represent unique plastid types. One can speculate that in these transitions ELIP plays a role similar to what it does during thylakoid biogenesis during de-etiolation, but for the reverse process of thylakoid disassembly. The precise details of this role remain to be determined, but the emerging recognition of the ubiquity of ELIP during different kinds of thylakoid dynamic states points to its importance in both normal developmental processes as well as in response to stress.
More remaining questions are where the ELIP protein is located during the massive membrane reorganization that occurs during plastid transitions, and how long it is required in the process. The northern blot data indicated a low but detectable level of ELIP mRNA in red ripe fruit, which is inconsistent with the high level of representation of ELIP cDNA in the EST collection (Table 1). Measurement of ELIP protein levels in these tissues will reveal if physiologically relevant amounts are present in chromoplasts. In chloroplasts subjected to high light stress, a thylakoid-associated serine protease degrades ELIP protein after the stress abates (Adamska et al., 1996). Given the loss of thylakoid structure during the transition to a chromoplast, the temporal and spatial location of the protease also becomes a relevant question.
The observation that ELIP mRNA is present during green fruit development is in agreement with observations made during barley leaf maturation (Grimm et al., 1989; Montané et al., 1997). Expression in developing green tissue most likely represents the requirement for ELIP protein during periods of intense chloroplast division accompanying fruit cell expansion (Gillaspy et al., 1993).
Published reports indicate that light regulation of ELIP gene expression is complex (reviewed in Adamska, 1997). There is evidence that phytochrome A (PhyA) mediates expression during the de-etiolation of seedlings (Adamska, 1995, 1997; Harari-Steinberg et al., 2001; Ma et al., 2001). PhyA has also been implicated in the process of lycopene accumulation in tomato fruit in the breaker to post-breaker stages of development, and the ratio of red to far-red light reaching pericarp tissue shifts between the immature green, breaker, and ripe stages. However, the chloroplast-to-chromoplast transition can occur in mature green fruit even in the absence of light (Alba et al., 2000). Many ripening-related genes are regulated by ethylene production, which peaks in the pre-breaker stage (reviewed in Zegzouti et al., 1999; Giovannoni, 2001; Alexander and Grierson, 2002). It is likely that ELIP gene expression is responsive to a variety of signals depending on the physiological process invoked by the signal. Further investigation into the signals required for ELIP expression in tomato fruit is underway.
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Acknowledgements |
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Funding for this project was provided by US Department of Energy grants DE-FG02-02ER15333 (Smith College) and DE-FG02-99ER20333 (East Tennessee State University) to CMW, and AKB was supported by a Sally Wilens Graduate Fellowship at Smith College.
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