Journal of Experimental Botany, Vol. 54, No. 381, pp. 375-383,
January 2, 2003
© 2003 Oxford University Press
The abundance of minor chlorophyll a/b-binding proteins CP29 and LHCI of barley (Hordeum vulgare L.) during leaf senescence is controlled by light
Received 31 May 2002; Accepted 4 August 2002
1 Institute of Plant Physiology, Martin-Luther-Universität Halle-Wittenberg, Weinbergweg 10, D-06120 Halle (Saale), Germany
2 Institute of Botany, Christian-Albrechts Universität Kiel, Am Botanischen Garten 1-9, D-24118 Kiel, Germany
3 To whom correspondence should be addressed. Fax: +49 345 55 27245. E-mail: humbeck{at}pflanzenphys.uni-halle.de
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Abstract |
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The abundance of the minor light-harvesting complexes CP29 and LHCI generally declines during the senescence of barley leaves. When light intensity declined due to clouding during the senescence of flag leaves from barley plants grown under field conditions, the levels of both light-harvesting complexes temporarily increased in parallel with photosystem II-efficiency [Fv/Fm]. A sudden shift from high light conditions to low light conditions during the growth of barley plants in a growth chamber also resulted in an increase in the abundance of minor light-harvesting complexes and a parallel increase in Fv/Fm as well as in the chlorophyll a+b-content of senescing primary foliage leaves. Northern blot analyses with a cDNA probe specific for the barley Lhcb4 gene encoding CP29 showed that the light-dependent changes in the abundance of CP29 during senescence are paralleled by corresponding changes in the transcript level. The results indicate that adjustments of the levels of minor light-harvesting complexes during senescence under high light conditions may serve in the prevention of photo-oxidative damage to the photosynthetic reaction centres and under low light in ensuring efficient photosynthesis of the residual photosynthetic reaction centres.
Key words: Barley, chlorophyll a/b-binding proteins, CP29, Hordeum vulgare, Lhcb4, LHCI, leaf senescence.
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Introduction |
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Leaf senescence is a developmental phase which follows the stage when leaves have achieved their final lengths and their maximal photosynthetic capacity (Gan and Amasino 1997; Noodén et al., 1997). Many investigations have shown that leaf senescence is not simply a passive ageing process, but rather is a complex developmental programme involving highly co-ordinated changes in cell structure, metabolism, function, and gene expression (Woolhouse, 1987; Smart, 1994; Nam, 1997; Quirino et al., 2000). This programme, as with many other developmental programmes, can be modulated by environmental conditions. Besides the availability of water and nutrients the light environment plays an important role (Stoddart and Thomas, 1982; Smart, 1994; Gan and Amasino, 1997; Weaver and Amasino 2001). The acclimation of leaves to the light environment is a well-known phenomenon. Besides responses at the level of the leaf (e.g. adjustment of numbers of chloroplasts per unit leaf area) there are several mechanisms of short- and long-term regulation at the level of the chloroplast (Horton et al., 1996). Long-term responses to changes in light intensity (termed acclimation) include the modulation of structure and function of the photosynthetic apparatus (Anderson et al., 1995). For example, de la Torre and Burkey (1990a, b) could show an increase in the Chl a/b-ratio after irradiation of barley with high light when compared to low light, which indicates a decrease in PSII antenna size in addition to changes in photosynthetic function. An extensive investigation on changes in light-harvesting complexes after growth at various light intensities by Bailey et al. (2001) revealed that there are multiple regulatory mechanisms underlying the acclimation of mature leaves of Arabidopsis thaliana to the light environment.
While Bailey et al. (2001) and others used mature leaves with high photosynthetic capacity for their studies, in the present report the focus is on the response of the photosynthetic apparatus in barley leaves to changes in ambient light intensity during the phase of senescence. One of the most characteristic features of leaf senescence is the dismantling of chloroplasts, including the degradation of the different protein components of the photosynthetic apparatus. The chloroplasts of senescing leaves are in a dilemma situation (Krupinska and Humbeck, 2003): on one hand photosynthesis is continuing for energy production and on the other hand the components of the photosynthetic apparatus are degraded. As also indicated by other investigations, efficient protection mechanisms dissipating excess excitation energy and an efficient control of energy-flow are required for the prevention of premature damage in senescing leaves (Feild et al., 2001; Lu et al., 2001; Ye et al., 2000; Casano et al., 1994). It has been proposed that minor light-harvesting complexes, especially CP29, play a pivotal role for the control of energy flow to the photosynthetic reactions centres (Jansson, 1994; Bassi et al., 1997). In the present report the abundances of the nuclear-encoded minor light-harvesting complexes of photosystem II (CP29, Lhcb4) and photosystem I (LHCI, Lhca2) were investigated during the senescence of barley leaves. The studies were performed with barley plants either grown under natural conditions in a field or under controlled environmental conditions in a climate chamber. The results show that, during senescence, the abundance of minor light-harvesting complexes is adjusted by light intensity. While the level of proteins generally decreases during senescence, the levels of the minor light-harvesting complexes in parallel to the photosynthetic efficiency temporarily increased when light intensity declined. To investigate whether light-dependent changes in CP29 protein levels are regulated at the transcript level, a cDNA specific for the barley Lhcb4 gene encoding CP29 was used for Northern blot analyses. The results indicate that changes in the levels of the CP29 protein coincide with parallel changes in the level of the corresponding transcript.
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Materials and methods |
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Plant material
Barley (Hordeum vulgare L.) was grown either under agricultural conditions in a field (Humbeck et al., 1996) or under controlled growth chamber conditions in ‘Mitscherlich’ pots on soil containing 4 g l–1 Chrysal (Multicote, Pakan and Chrysal, Naarden, The Netherlands). In the field trials flag leaves of different developmental stages were collected between 10.00 h and 12.00 h. Samples were either used directly for measurements of photosynthetic parameters and chlorophyll content or were immediately frozen and transported to the laboratory in liquid nitrogen and then stored at –80 °C. Cultivation of barley plants, cv. Trixi, in a growth chamber was performed in a daily light/dark regime (16/8 h light/dark) as described previously (Kleber-Janke and Krupinska, 1997). Measurements of photosynthesis parameters and collections of primary foliage leaves were done in the middle of the light period, respectively. For further biochemical and molecular analyses, whole leaves were immediately frozen in liquid nitrogen and then stored at –80 °C.
Photosynthetically active radiation (PAR)
To monitor changes in photosynthetically active radiation (PAR, µmol m–2 s–1) a meteorological station with a data-logging device (LI-1000, Li-cor, Walz, Effeltrich, Germany) was established in the field. The amount of quanta (PAR) per 24 h and m–2, respectively, were integrated.
Photosynthetic capacity
Photosynthetic oxygen evolution was measured with a leaf-disc O2-electrode (HansaTech, Kings Lynn, Norfolk, UK; model LD1 with a LS2 light source) at 20 °C as previously described (Humbeck et al., 1996). Each single measurement was made on three leaf segments excised from the mid-part of the leaves, each 1.5 cm in length. A saturating light intensity of 2050 µmol m–2 s–1 was used for the determination of photosynthetic capacity.
Chlorophyll fluorescence measurements
Chlorophyll fluorescence parameters were measured using a pulse amplitude modulation fluorometer (Mini-PAM, Walz, Effeltrich, Germany) according to the instructions given by Schreiber et al. (1986). Measurements were performed at the mid positions of intact leaves. For each measurement, 10 different leaves were used. Prior to fluorescence measurements, the leaf blades were dark adapted for 30 min. F0 was measured with modulated light (1.6 kHz) of approximately 0.1 µmol m–2 s–1. This intensity is sufficiently low not to produce any significant Fv. Maximal fluorescence (Fm) was determined by application of a saturating flash of white light (4000 µmol m–2 s–1) of 700 ms duration. The Fv/Fm ratio which is a measure of the quantum yield of photosystem II photochemistry, was determined as (Fm–F0)/Fm (Butler, 1977).
Chlorophyll content
Relative chlorophyll content per unit leaf area was determined using a SPAD (Soil Plant Analysis Development) analyser (Minolta, by Hydro Agri, Dülmen, Germany) which measures transmission of wavelengths absorbed by chlorophylls in intact leaves (mid position). Relative SPAD values depend on chlorophyll content in a linear manner over a wide range. Each data point represents the mean value of 10 independent measurements.
The chlorophyll a/b-ratio was determined spectrophotometrically after gentle extraction of pigments with methanol using the formula given by Lichtenthaler (1987).
Isolation and analysis of RNA
Total RNA was isolated as described (Chirgwin et al., 1979) and fractionated on 1% (w/v) agarose gels containing formaldehyde. The RNA was then transferred onto positively charged nylon membranes (Zeta probe; BioRad, München, Germany) by capillary blotting.
For analysis of Lhcb4 mRNA levels, the cDNA HvCP29 was used. The cDNA clone was obtained by differential screening of a Lambda ZAPII (Stratagene, Europe, Amsterdam, The Netherlands) cDNA library prepared from RNA of barley flag leaves harvested on day 2 before the onset of senescence (Humbeck et al., 1996) with cDNA probes representing gene expression 4 d before and 2 d after the onset of senescence, respectively. Sequence analyses revealed that one of the cDNA clones hybridizing preferentially with the cDNA probe from mature flag leaves harvested before the onset of senescence is specific for the Lhcb4 gene encoding the chlorophyll a/b-binding protein CP29. The 447 bp nucleotide sequence of the partial cDNA was added to the EMBL database (Accession No. AJ006296). The cDNA probe was radio-labelled with [
-32P]dCTP using a random primed labelling kit (Boehringer, Mannheim, Germany).
The membranes were prehybridized at 42 °C for 5 min in a solution consisting of 50% (v/v) deionized formamide, 0.25 M sodium hydrogen phosphate, pH 7.2, 0.25 M sodium chloride, 1 mM EDTA, and 7% (w/v) SDS. Hybridization was carried out overnight at 42 °C in the same solution after addition of the radiolabelled Lhcb4 probe. After the filters were washed, they were autoradiographed using KODAK X-OMAT, AR films (Eastman Kodak, Rochester, NY).
Immunological analysis of protein levels
Proteins were extracted from whole leaf blades as described earlier (Humbeck et al., 1996). Equal amounts of proteins (30 µg) were subjected to SDS-PAGE according to Humbeck et al. (1994). Separated proteins were transferred to nitrocellulose filters (Schleicher and Schüll, Dassel, Germany) by electroblotting. The blot was incubated with the primary antibody and immunoreactive bands were visualized using a peroxidase coupled antiserum with chemiluminescence detection (Amersham, Braunschweig, Germany). A monoclonal antibody directed towards LHCI (24 kDa) had been prepared previously and shown to cross-react with CP29 (Hoyer-Hansen et al., 1988). Protein components of LHCII were immunologically detected using an antibody described by Harrison and Melis (1992).
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Results |
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Changes in the abundances of CP29 and LHCI during maturation and senescence of flag leaves from field-grown barley plants
The abundances of CP29 and LHC1 were examined during maturation and senescence of flag leaves from barley plants grown under field conditions (Humbeck et al., 1996). For immunological analyses a monoclonal antibody directed originally towards LHCI of photosystem I of barley (24 kDa) and shown to cross-react with CP29 (Hoyer-Hansen et al., 1988) was used. Proteins were analysed from flag leaves of winter barley (Hordeum vulgare L. cv. Trixi) grown under field conditions. In this specific field trial the onset of senescence (sample 0), as shown by a decrease in Fv/Fm (Fig. 1), occurred about 23 d post anthesis. As also shown previously for other photosynthesis related proteins the levels of both minor light-harvesting complexes, CP29 and LHCI, were high before the onset of senescence and dramatically decreased thereafter. In this field trial the abundance of CP29 and LHCI temporarily increased on day 4 after the onset of senescence, in parallel with an increase in Fv/Fm (Fig. 1). It is feasible that this reversion of senescence-related degradation was caused by a transient decrease in photosynthetically active radiation (PAR) due to clouding on days 3 and 4 after the onset of senescence. On day 6 after the onset of senescence PAR was again high and the senescence specific decrease in Fv/Fm continued. The changes in Fv/Fm (Fig. 1) and in photosynthetic capacity, i.e. oxygen evolution at saturating light intensities, and chlorophyll content (Fig. 2), indicate a transient reversion of at least some senescence processes on day 4 after the senescence onset. Immunological analyses revealed that the levels of both inner light-harvesting complexes associated with photosystem II (CP29) and photosystem I (LHCI), respectively, were regulated in a similar fashion (Fig. 1). As shown in Fig. 2, levels of LHCII also generally decreased during leaf senescence. In total, the three apoproteins detected by the LHCII-antibody gradually decreased and, except for the upper band, showed no pronounced transient increase on day 4 after the onset of senescence. In parallel to the decrease in LHCII, the chlorophyll a/b-ratio slightly increased during senescence (Fig. 2). On day 4 after the onset of senescence when levels of minor LHCs transiently increased again, this value correspondingly slightly decreased in a transient fashion.
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RNA analyses with a barley cDNA probe specific for the Lhcb4 gene encoding CP29
To investigate whether the effect of light on the abundance of minor light-harvesting complexes during senescence is exerted at the level of transcript accumulation, Northern blot analyses with RNA from flag leaves of barley plants grown in a field trial similar to that shown in Fig. 1 were performed. The cDNA probe used for hybridization was specific for the barley Lhcb4 gene encoding CP29 (see Materials and methods). This RNA analysis clearly showed that the Lhcb4 mRNA level was high in mature leaves and dramatically decreased after the onset of senescence (Fig. 3). Also in this field trial, the photosynthetic active radiation (PAR) was transiently decreased during the phase of leaf senescence. As already shown for the CP29 protein level, the decrease in PAR coincided with a temporary increase in the Lhcb4 mRNA level.
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Effects of light intensity on photosynthesis parameters and the abundances of CP29 and LHCI in primary foliage leaves of barley grown under controlled environmental conditions in climate chambers
To investigate whether the observed transient reversion of the senescence-related decrease of CP29 and LHCI levels in barley flag leaves was indeed caused by the change in light intensity, a similar situation was experimentally applied to barley primary foliage leaves of plants grown under controlled environmental conditions in climate chambers (Miersch et al., 2000). In this case, barley plants were grown either at low light intensity (100 µmol m–2 s–1) or at high light intensity (1000 µmol m–2 s–1). While at low light intensity, the photosystem II efficiency (Fv/Fm) of primary foliage leaves stayed high until day 30 after sowing and then sharply decreased (Fig. 4A), at high light intensity the development of the leaves was accelerated as shown by an earlier onset of senescence on day 17 after sowing. When, on day 25 after sowing, some of the plants were transferred from high to low light conditions, a transient increase in photosystem II efficiency from Fv/Fm=0.51 on day 25 to Fv/Fm=0.68 on day 28 was observed. Beyond day 28 after sowing, the Fv/Fm ratio again decreased and reached a value close to zero as in the high light-treated plants. By comparison, plants kept under the high light conditions showed a continuous decrease in Fv/Fm from 0.51 on day 25 to 0.30 on day 28 after sowing. As already reported before (Miersch et al., 2000), chlorophyll content began to decrease at the early stages of leaf development and under low light conditions reached values close to zero 46 d after sowing (Fig. 4B). High light treatment resulted in a slightly higher chlorophyll content in the early phases of leaf development. In high light conditions, chlorophyll is degraded much faster than in the low light control and reached a value close to zero already on day 32 after sowing. A transfer from high to low light intensities on day 25 after sowing coincided with a transient increase in chlorophyll content. Compared with the increase in Fv/Fm, the increase in chlorophyll content was slower showing a peak on day 30 after sowing.
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To investigate whether the changes in photosystem II efficiency and chlorophyll content are accompanied by corresponding changes in the levels of CP29 and LHCI, immunological analyses were performed (Fig. 5). In the high-light-treated samples both inner light-harvesting complexes were clearly down-regulated during senescence. Transfer of the plants from high light intensity to low light intensity on day 25 after sowing induced a dramatic up-regulation of the levels of both complexes, CP29 and LHCI, both having a maximal level on day 30. Thereafter, the levels of both proteins quickly declined.
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Discussion |
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During senescence chloroplasts fulfil two contrasting functions. On the one hand, components of the photosynthetic apparatus are degraded for the remobilization and recycling of N-compounds and other valuable substances. On the other hand, photosynthesis is still going on to ensure the production of the assimilates required for the growth of sink organs as well as the synthesis of ATP as an energy source for the breakdown processes within the senescing leaf. Under these conditions effective mechanisms to protect the photosynthetic apparatus from photo-oxidative damage are required (Feild et al., 2001; Lu et al., 2001; Ye et al., 2000; Casano et al., 1994).
In the present report, the focus has been on the inner light-harvesting complexes CP29 and LHCI of PSII and PSI, respectively, which, apart from their light-harvesting function, are thought to play a pivotal role for the protection of photosynthetic reaction centres against the harmful effects of excess light by regulating the energy flow within the photosystems (Bassi et al., 1997). The inner light-harvesting complexes of PSII are proposed to channel absorbed light energy from the peripheral antenna LHCII towards the core of photosystem II (Bassi et al., 1997). Several mechanisms for the regulation of this energy flow have been suggested, for example, the induction of a trans-thylakoid 
pH resulting in conformational changes affecting energy transfer (Ruban et al., 1996, 1998), or the dissipation of excess energy via zeaxanthin formed from violaxanthin (Havaux et al., 2000; Crimi et al., 2001). It has been shown that the minor light-harvesting complexes indeed bind a high proportion of the xanthophyll cycle pigments (violaxanthin and zeaxanthin) (Gilmore et al., 1998; Verhoeven et al., 1999) and that CP29 is a possible target for phosphorylation, which could be part of a mechanism that quickly regulates energy flow to photosystem II reaction centres, thereby preventing photoinhibition under stress conditions (Bergantino et al., 1998). However, the exact function of the phosphorylated CP29 is still a matter of debate (Buffoni et al., 1998< 1998).
In mature leaves possessing chloroplasts with high photosynthetic capacity, changes in photosynthetically active radiation from low to high values measured in the field did not significantly affect photosystem II efficiency and the levels of CP29 and LHCI (Fig. 1), indicating that during this period the photosynthetic apparatus was sufficiently protected against photodamage by the above-mentioned processes or by additional protection mechanisms. These results are in agreement with data reported by Bailey et al. (2001) who immunologically investigated levels of all chlorophyll b-binding proteins in mature leaves of Arabidopsis after growth at various light intensities. The mature Arabidopsis leaves show also no pronounced response of minor LHCs CP29 (Lhcb4) and LHCI (Lhca2) to growth light intensity.
At the onset of senescence the situation dramatically changes. The photosynthetic apparatus which, up to that stage, very efficiently utilized light in a wide range of fluence rates is now degraded. This is reflected by a sharp decrease in photosystem II efficiency indicating the functional disorganization of photosystem II caused by the breakdown of its components during leaf senescence (Humbeck et al., 1996). The levels of the two minor light-harvesting complexes CP29 and LHCI dramatically decrease during senescence (Figs 1, 5). In this respect these proteins behave as other proteins of the photosynthetic apparatus (Humbeck et al., 1996; Miersch et al., 2000), for example, LHCII (Fig. 2). By contrast with the levels of the latter proteins, the levels of the minor LHCs during leaf senescence respond positively to changes in ambient light intensity (Figs 1, 5).
These studies show that during senescence the levels of CP29 and LHCI are controlled by light intensity. They increased transiently when, during senescence, ambient light intensity temporarily decreased either due to clouding under field conditions (Fig. 1) or when light intensity of the growth chamber intentionally was decreased (Fig. 5). The increase in the levels of the two proteins was paralleled by an increase in photosynthetic capacity and photosystem II efficiency (Figs 1, 2, 4). The results presented in this paper show that chloroplasts are obviously able to switch at least parts of their senescence programme from degradation and recycling to reconstruction of the photosynthetic machinery in response to a decrease in ambient light intensity. Comparable results have been reported by Hidema et al. (1992) who showed that the degradation of light-harvesting complexes during senescence is delayed under low irradiances and by Ahn et al. (1994) who showed that levels of light-harvesting complexes are clearly reduced in high-light-treated plants when compared to the low-light-treated plants.
The results suggest that the senescence-specific degradation of the photosynthetic apparatus as shown by a decrease in the levels of both minor LHCs, CP29 and LHCI, and by decreasing photosynthetic activities may be modulated by external factors such as light intensity (Figs 1, 5). It is likely that, during senescence, adjustments of the amounts of CP29 and LHCI, in addition to the above-mentioned mechanisms, play an important role for photoprotection of the photosystems. This mechanism may help to overcome the problems associated with the dilemma situation of the senescing chloroplasts. Under high light intensity a fast decrease in abundance of these complexes may restrict energy flow to the photosystems. Under low light intensity a high level of these complexes ensures efficient photosynthesis of the remaining photosystems.
Both the senescence-specific decrease and the light-dependent transient increase in CP29, correlate with corresponding changes in the transcript level specific for the Lhcb4 gene encoding CP29. These data suggest that developmental and environmental regulation of CP29 abundance is at least in part regulated at the transcript level.
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Acknowledgements |
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We thank Dr David Simpson (Carlsberg Research Centre, Copenhagen, Denmark) and Dr Anastasios Melis (University of California, Berkeley, USA) for providing the antibodies specific for LHCI and CP29 and for LHCII. Dr. Sabine Quast and Dr Jon Falk are thanked for isolation and sequence analysis of the cDNA HvCP29 of barley. This research was supported by the Bundesministerium für Forschung und Technologie (BEO 031 6601) and the Deutsche Forschungsgemeinschaft (Kr 1350/3).
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A. Wingler, E. Brownhill, and N. Pourtau Mechanisms of the light-dependent induction of cell death in tobacco plants with delayed senescence J. Exp. Bot., November 1, 2005; 56(421): 2897 - 2905. [Abstract] [Full Text] [PDF]
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