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First published online September 14, 2007; 10.1104/pp.107.106336 Plant Physiology 145:691-702 (2007) © 2007 American Society of Plant Biologists Dual Role of the Plastid Terminal Oxidase in TomatoCentre National de la Recherche Scientifique and Université Joseph Fourier, Laboratory Plastes et Différenciation Cellulaire, 38041 Grenoble, France (M.S., A.-M.L., M.K.); and Institut für Biologie I, Pflanzenphysiologie, Universität Leipzig, D–04103 Leipzig, Germany (M.G.)
The plastid terminal oxidase (PTOX) is a plastoquinol oxidase whose absence in tomato (Solanum lycopersicum) results in the ghost (gh) phenotype characterized by variegated leaves (with green and bleached sectors) and by carotenoid-deficient ripe fruit. We show that PTOX deficiency leads to photobleaching in cotyledons exposed to high light primarily as a consequence of reduced ability to synthesize carotenoids in the gh mutant, which is consistent with the known role of PTOX as a phytoene desaturase cofactor. In contrast, when entirely green adult leaves from gh were produced and submitted to photobleaching high light conditions, no evidence for a deficiency in carotenoid biosynthesis was obtained. Rather, consistent evidence indicates that the absence of PTOX renders the tomato leaf photosynthetic apparatus more sensitive to light via a disturbance of the plastoquinone redox status. Although gh fruit are normally bleached (most likely as a consequence of a deficiency in carotenoid biosynthesis at an early developmental stage), green adult fruit could be obtained and submitted to photobleaching high light conditions. Again, our data suggest a role of PTOX in the regulation of photosynthetic electron transport in adult green fruit, rather than a role principally devoted to carotenoid biosynthesis. In contrast, ripening fruit are primarily dependent on PTOX and on plastid integrity for carotenoid desaturation. In summary, our data show a dual role for PTOX. Its activity is necessary for efficient carotenoid desaturation in some organs at some developmental stages, but not all, suggesting the existence of a PTOX-independent pathway for plastoquinol reoxidation in association with phytoene desaturase. As a second role, PTOX is implicated in a chlororespiratory mechanism in green tissues.
The plastid terminal oxidase (PTOX) is a nucleus-encoded plastid-located plastoquinone (PQ)-O2 oxidoreductase (plastoquinol oxidase) whose absence gives rise to the immutans phenotype in Arabidopsis (Arabidopsis thaliana) and in the ghost (gh) phenotype in tomato (Solanum lycopersicum; Carol et al., 1999  ; Wu et al., 1999; Josse et al., 2000; Carol and Kuntz, 2001; Rodermel, 2001; Aluru et al., 2006). These phenotypes are characterized by variegated leaves consisting of green and bleached sectors and, in addition in tomato, by a yellow-orangey ripe fruit. The latter is characterized by reduced carotenoid content (Barr et al., 2004). In addition, bleached leaf sectors accumulate the carotenoid precursor phytoene, indicating that PTOX functions as a cofactor for the carotenoid dehydrogenases, namely, phytoene desaturase (PDS) and, most likely,  -carotene desaturase (ZDS). These conclusions are consistent with the known involvement of quinone as a cofactor for PDS (Mayer et al., 1990; Norris et al., 1995). PDS and ZDS sequentially catalyze the conversion of the colorless phytoene to lycopene (the main pigment in red tomato fruit), which, in turn, is converted to various photoprotective carotenoids. Thus, the phenotype observed in the absence of PTOX can be explained by reduced ability to synthesize carotenoids leading to photobleaching of green tissues.
PTOX shares sequence similarity with the alternative oxidase found in mitochondria of a number of species (Berthold and Stenmark, 2003 In this article, various tomato organs were used under experimental conditions leading to photobleaching to examine in the absence of PTOX whether this phenomenon is linked to abnormal carotenoid content or to abnormal photosynthetic electron transport. A potential influence of PTOX on the redox status of the PQ pool was also examined.
Effect of PTOX Deficiency in gh Tomato Cotyledons
‘San Marzano’ (SM) control and gh seedlings were grown in darkness for 4 d after seed imbibition (time point T0). These white seedlings were then transferred to either low or high light conditions for 24 h. As shown in Figure 1A
, at T0, cotyledons from both SM and gh were almost devoid of chlorophyll and carotenoid (mainly lutein and violaxanthin) levels were low, but slightly higher in SM than in gh. Within the low light period, both cotyledon types accumulated substantial amounts of chlorophyll a/b and carotenoids (including
Under high light conditions (Fig. 1A), a slightly higher level (not statistically significant) of pigments was observed in SM (including the xanthophyll cycle pigments antheraxanthin and zeaxanthin; A + Z) when compared to low light, whereas this increase was not observed in gh (chlorophyll content is even reduced in gh under high light compared to low light). The carotenoid precursor phytoene was not detected in SM under any condition, but was present (as two isomers) in gh at T0 (Fig. 1A). A rise in phytoene level was observed in gh under low light but was not statistically significant. Accumulation of phytoene is most likely the result of two parameters: (1) the activity of the whole biosynthetic pathway; and (2) the limiting rate of PDS activity in the absence of PTOX. However, phytoene levels in gh were lower under high light than under low light (statistically significant; P < 0.01), despite the fact that the carotenoid biosynthetic pathway seems active under high light (as deduced from the high levels of colored carotenoid in SM). Because lower levels of colored carotenoids and chlorophyll are also found in gh under high light versus low light, the simplest explanation for these observations is increased photodestruction of all these compounds. Seedlings grown for a longer period (6 d) in darkness (Fig. 1B, time point T0) showed a faint yellow color. Significantly higher carotenoid levels were present in SM than in gh. The same low or high light conditions were then applied during 6 h. Low light led to an increase in chlorophyll and carotenoid levels, with no significant difference between SM and gh. Compared to low light, high light triggered again a slight increase (not statistically significant) in pigment levels in SM. In gh, significantly lower pigment levels were observed under high light compared to SM. In addition, its phytoene levels under high light were lower than at T0 (statistically significant; P < 0.01), which can be explained in part by photodestruction. The fact that lower levels of phytoene were also observed in gh under low light at 6 h than at T0 (statistically significant; P < 0.05) is more surprising and may suggest that carotenoid biosynthesis is less active (because almost-normal carotenoid content was reached; see Fig. 1B). Taken together, these data suggest that PTOX deficiency leads to photobleaching in cotyledons exposed to high light primarily as a consequence of reduced ability to synthesize colored carotenoids in the mutant, which is fully consistent with the known role of PTOX as a PDS cofactor.
When grown under standard growth chamber conditions, SM and gh plants produce green and variegated leaves, respectively. The color aspect of gh leaves is decided at a very early leaf developmental stage. Depending on light intensities at an early seedling developmental stage (see "Materials and Methods"), gh leaves, which are mainly green, mainly white, or variegated, could be obtained (Fig. 2A
, inset). Mainly white leaves (of adult size) showed clear reduction in chlorophyll a/b and carotenoids (neoxanthin, violaxanthin, lutein, and
Detached fully green leaves (with no visible deficit in pigments, as shown in Fig. 2A, sample 2) were then exposed to high light (1,000 µmol m–2 s–1) for long incubation periods. Leaves from both SM and gh showed early bleaching symptoms in some sectors after 20 to 24 h. This trend appears earlier and is stronger in gh (Fig. 2D, inset) and extends to larger leaf sectors with longer incubation time. Pigments were extracted separately from green and bleaching sectors. As expected, these leaves showed accumulation of the xanthophyll cycle pigments A + Z (data not shown) and bleaching sectors contained reduced chlorophyll and carotenoid content. This reduction was more pronounced in gh than in SM. However, an unexpected observation was that phytoene was not detected in any tissues in contrast to what was observed in cotyledons (Fig. 1) or mainly white or variegated leaves (Fig. 2C). Figure 2D compares typical HPLC elution profiles from a bleached sector after 24 h of high light and from a mainly white leaf whose aspect is determined early during leaf development (as shown in Fig. 2A). To shed more light on changes occurring in chloroplasts under these experimental conditions, a series of experiments were performed at earlier time points (before bleaching was visible). First, pigment analyses (Table I ) were performed using plants grown under low light (60 µmol m–2 s–1) conditions (T0), and then green leaves were detached and incubated either under low light (60 µmol m–2 s–1) or high light (1,000 µmol m–2 s–1) for 6 h (T6h) or 16 h (T16h). At T6h under low light, only marginal changes in pigment content were observed with respect to T0 in both SM and gh leaves, with the exception of an increase in the levels of xanthophyll A + Z for both SM and gh. This increase was unexpected because this light intensity is identical to that experienced by the plants before these experiments and is most likely due to the detachment of leaves. At T6h under high light conditions, higher A + Z levels were observed, as expected, and, interestingly, with a stronger increase in SM versus gh. No other significant change in pigment content was observed at T6h under high light, with the exception of a decrease in violaxanthin, the precursor of A + Z during activation of the xanthophyll cycle. Compared to T6h, at T16h under high light conditions, the most notable change was an increase in A + Z levels in gh, which equaled the levels in SM (data not shown). No phytoene was detected in any sample.
Proteins were extracted from leaves at T0 and over a time course up to T16h, under either low or high light. Immunodetection did not reveal any signal for PTOX in gh (data not shown), as expected, but a 37-kD band was visible in SM (Fig. 3A ). High light conditions led to a gradual rise in PTOX level in SM (which is particularly evident at T16h). Under low light, only a slight increase with time is apparent (most likely due to leaf detachment). The PSI-D polypeptide level was not found to change during this time course and can therefore be considered an internal control to ensure equal gel loading. Figure 3B shows the densitometric scanning of the PTOX band from Figure 3A after normalization using the PSI-D band as a standard.
The maximal quantum yield of PSII was estimated from the Fv/Fm ratio. At T6h, under high light (Fig. 4 ), the Fv/Fm ratio was found to decrease, as expected, under these photoinhibitory conditions in both SM and gh leaves (but more in gh). The same observations were made when the temperature was shifted to 15°C instead of 24°C: Again, gh leaves showed a lower Fv/Fm ratio than SM leaves under high light (Fig. 4). At T16h, the further decrease in Fv/Fm was also stronger in gh than in SM leaves (data not shown).
Lipid peroxidation was estimated using the malondialdehyde (MDA) method over a 6-h time course after transfer of leaves to high light. These data (Fig. 5A ) suggest an increase in lipid peroxidation in both gh and SM, but greater in gh.
Thermoluminescence measurements were performed on attached green leaves directly after 6 h of high light stress and after an additional 24-h recovery period under low light conditions. As controls, leaves maintained for 6 h under low light were used. Thermoluminescence glow curves (Ducruet, 2003 ) show a B band peaking at 25°C and a high temperature band peaking at 130°C to 140°C (HTL2; representing the oxidative stress of leaves). As shown in Figure 5B (left), the B band is shifted after light stress to a position corresponding to a lower temperature with a 43% decrease in light-stressed SM leaves, indicating photoinhibition and damage to PSII. After 24 h of recovery, the B band resumes its initial amplitude and peak position. In light-stressed gh leaves, a decrease of 78% is observed for the B band, also accompanied by a shift to lower temperature, but after 24 h of recovery the B band regenerated only to 70% compared to control leaves and the peak shift was still visible (Fig. 5B, right). No increase in the HTL2 band was visible after 6 h of light stress in SM leaves (Fig. 5B). In contrast, the HTL2 band was 150% higher in light-stressed gh leaves compared to control leaves (significant at P < 0.01). After 24 h of recovery, a further increase was observed in gh, but an increase was also observed in SM at that time point in comparison to 6 h of light stress (see "Discussion"). It therefore appears that the absence of PTOX renders the tomato leaf photosynthetic apparatus more sensitive to extreme conditions (provided here by a transfer to excessive light). This increased sensitivity is observed in the absence of any detectable accumulation of phytoene or decrease in carotenoid content.
Fast fluorescence kinetics (OJIP, also called OI1I2P; Schreiber, 2004
In another set of experiments, induction kinetics of chlorophyll fluorescence were performed over a longer time range after 30-min incubation of leaves in the dark followed by exposure to actinic light (200 µmol m–2 s–1) for 10 min (Fig. 7 ). In this time window, the Kautsky kinetic describes the drop of the fluorescence from the Fm level (P level) to the steady-state level (Fs) and is characterized by the complex superposition of processes, including the light-induced activation of PSI, the Calvin cycle, alternative electron transfer (e.g. Mehler reaction), and buildup of  pH-dependent nonphotochemical quenching (qN). Consistent results were obtained showing that the effective quantum yield of PSII ( PSII) is lower in gh versus SM and that the relative reduction state of QA (estimated as 1 – photochemical quenching parameter [qP]) is higher in gh versus SM. 1 – qP also reflects the overall reduction state of the electron transport chain and therefore the quinone pool. When this parameter was expressed as 1 – qL (Kramer et al., 2004), the same result was obtained (data not shown). In contrast, qN was not found to differ significantly between both leaf types.
Effect of PTOX Deficiency in Tomato Fruit
Young tomato fruit bleach in the gh line under standard greenhouse conditions or show a variegated green/white color under shaded conditions (Barr et al., 2004
Explants from mature green fruit were incubated under 1,000 µmol m–2 s–1 for up to 48 h at 24°C. Bleaching symptoms were observed after approximately 24 h in both SM and gh explants, but were stronger in gh (data not shown). Analysis of their carotenoid content at various time points (6, 18, 30, and 42 h) revealed no phytoene (data not shown), indicating that the absence of PTOX does not limit carotenoid biosynthesis in these gh explants. Estimation of the maximal quantum yield of PSII after 6 h of incubation (Fig. 9 ) showed that gh fruit are more sensitive to photoinhibition than SM fruit under this high light condition at 24°C. At 15°C, both fruit types are fully photoinhibited under these light conditions.
Fully Greened Tissues Can Desaturate Carotenoids without PTOX Our data show that, in the absence of PTOX, the lower capacity to desaturate carotenoids is primarily responsible for the phenotype in cotyledons of dark-grown tomato gh seedlings and when these seedlings are transferred to light. These tissues have reduced colored carotenoid levels and accumulate their precursor phytoene. Considering the well-known photoprotective role of carotenoids, this pigment deficiency will lead to bleaching in tissues where assembly of the photosynthetic apparatus is initiated upon transfer to light. Although not studied here, it can be speculated that such a pigment deficit is also (at least partially) responsible for the variegated leaf phenotype that is initiated at an early chloroplast developmental stage (when optimal carotenoid biosynthesis is likely to be important). Consistent with this view, bleached sectors in variegated leaves contain phytoene. However, an additional role for PTOX in photosynthetic electron transport (see below) during the buildup of the photosynthetic apparatus cannot be excluded.
In contrast, when normal chloroplast biogenesis was not impaired (i.e. when excessive light was avoided at an early stage), different observations were made in gh green adult leaves: We were unable to detect phytoene (nor a deficit in carotenoid content) even under such excessive light ultimately leading to bleaching. This is highly surprising because the carotenoid biosynthetic pathway is likely to be very active under such conditions to compensate for carotenoid turnover and photodestruction (Simkin et al., 2003
Our data consistently suggest that PTOX plays a specific role in the protection of the fully assembled photosynthetic apparatus under light constraints. We used adult leaves subjected to severe light conditions, which led to photobleaching after prolonged incubation (24 h) in both gh and control SM lines. Such prolonged light exposure and provoked photobleaching are not normal phenomena in nature but were used here to ensure that the applied conditions were creating extreme constraints. We then used earlier time points compatible with a normal photoperiod for detailed investigation. These indicated higher PSII photoinhibition in gh versus SM leaves after 6 h (Fig. 4) and 16 h of light stress (data not shown), as well as higher damage level of PSII in gh than in SM and only partial recovery in gh (thermoluminescence B band; Fig. 5B). High-temperature thermoluminescence measurements (HTL2 band; Vavilin and Ducruet 1998
In vitro, PTOX is a plastoquinol oxidase (Josse et al., 2000
In addition, fast fluorescence induction kinetics (Fig. 6) show that PTOX regulates the reduction state of the PQ pool in the dark. The increased amplitude of the J level indicates that a more strongly reduced PQ pool is present in gh, the extent of which depends on the duration of the dark incubation prior to pulse illumination. The simplest way to interpret these results is to assume that, in the absence of PTOX, the NAD(P)H dehydrogenase (NDH) complex strongly reduces PQs in the first 30 min in the dark. The decrease in the J level after 4 h in gh suggests that, over a long period of time, reoxidation of reduced PQs does occur in gh, either by pure chemical oxidation with molecular oxygen (Khorobrykh and Ivanov, 2002
Correlative evidence for PTOX as a bona fide safety valve (i.e. allowing the transfer of excess electrons to O2) is essentially provided for higher plants by gene expression/protein accumulation data (Rizhsky et al., 2002
Acclimation of plants to environment and its constantly changing conditions implies a highly sophisticated network of regulation, which seems to involve chlororespiration (Rumeau et al., 2007
A regulatory role for PTOX is also suggested by the slightly higher pigment content of green leaves in gh versus SM (Fig. 2, A and B). However, this slight increase in both chlorophyll and carotenoid content is unlikely to be the causal link between the lack of PTOX and the various effects on photosynthetic electron transport described here. For instance, in gh the influence of dark adaptation time on fast fluorescence kinetics (Fig. 6) or delay in full activation of the xanthophyll cycle during long incubation under severe light conditions (Table I) must result from more complex regulatory mechanisms. In addition, a rise in chlorophyll content was observed in quite similar proportions when wild-type and immutans Arabidopsis were compared (Rosso et al., 2006
As in leaves, bleaching of young gh fruit is determined at an early developmental stage. The presence of phytoene in white gh fruit suggests it is linked (at least partially) to a deficit in carotenoid biosynthesis. In contrast, the sensitivity to high light conditions of mature gh fruit that were maintained green could not be linked to a deficit in carotenoid biosynthesis. We found gh green fruit to be more susceptible to photoinhibition than SM control fruit, which again is similar to our observation in adult green gh leaves.
In ripening gh fruit derived from green fruit, the lycopene-synthesizing capacity of fruit is reduced compared to wild type, but is not zero, which may suggest that, in the absence of PTOX, another cofactor of carotenoid desaturase replaces PTOX. The identity of this cofactor (Carol and Kuntz, 2001
Bleaching at the green stage in gh fruit influences the capacity to synthesize carotenoids during fruit ripening: The amount of lycopene present in ripe fruit derived from white gh fruit is decreased 3-fold compared to ripe fruit derived from green gh fruit (Fig. 8E). Because carotenoid biosynthesis is catalyzed by membrane-bound enzymes and because bleached gh fruit are affected in their plastid ultrastructure (Barr et al., 2004
Plant Materials Tomato (Solanum lycopersicum) of SM genotype and its monogenic gh mutant (LA0259; Tomato Genetic Stock Center) were grown at 24°C with a 16-h photoperiod (white light, 60 µmol m–2 s–1). Seedlings were first grown at low light intensity (10 µmol m–2 s–1 for 1 week and then 20 µmol m–2 s–1 for 4 weeks) and then placed under the above-mentioned light conditions to obtain adult plants with green leaves for gh. Both white and variegated gh leaves were obtained by incubation of seedlings directly at 60 µmol m–2 s–1. For experiments with cotyledons, SM and gh seedlings were grown in darkness for 4 and 6 d after seed imbibition to obtain white and pale yellow cotyledons, respectively. Seedlings were then transferred to either low light (20 µmol m–2 s–1) or higher light intensities (200 µmol m–2 s–1). For light stress experiments, young (fully elongated) leaves or mature green fruit were harvested 3 to 4 h after the beginning of the photoperiod and incubated at 24°C under 60 µmol m–2 s–1 (control) and 1,000 µmol m–2 s–1 (stress).
Chlorophyll a fluorescence was measured with a pulse-modulated fluorometer (Walz) at room temperature. Leaves and fruits were kept in the dark for 30 min prior to the measurements. Variable fluorescence (Fv) was calculated as Fm – F0, where F0 is minimal fluorescence (under a weak measuring beam) and Fm maximal fluorescence (determined after an 800-ms saturating pulse of white light at 2,500 µmol m–2 s–1). Prior to fluorescence measurements, photoinhibitory conditions were obtained by exposing plant samples to an irradiance of 1,000 µmol m–2 s–1 for 6 or 16 h at 15°C or 24°C.
For experiments using prolonged illumination, actinic white light (200 µmol m–2 s–1) was used and saturating pulses were applied at 1-min intervals for 10 min to determine maximal fluorescence (F'm), steady-state fluorescence (Fs), and, after actinic light was switched off and a brief far-red pulse was applied, to measure minimal fluorescence (F'0). The coefficient qP was calculated as (F'm – Fs)/(F'm – F'0) (Schreiber et al., 1989
Fluorescence induction kinetic curves (OJIP) were measured with a Handy-PEA fluorometer (Hansatech) according to Strasser et al. (2004)
Thermoluminescence measurements were performed on 6-mm leaf discs as described previously (Gilbert et al., 2004
MDA assays were performed according to Hodges et al. (1999)
Total protein was extracted from frozen and ground material using the Hurkman and Tanaka method (Hurkman and Tanaka, 1986
Pigments were extracted from lyophilized samples (5-mg leaves or cotyledons, 10-mg fruit pericarp) using methanol (neutralized with 5 mM Tris-HCl, pH 7.0). In addition, fruit methanolic extracts were added with 1 volume of water and then phase partitioned with a volume of chloroform. The aqueous phase was re-extracted twice with chloroform and the pigments dried from the pooled chloroform phases. The HPLC method used to analyze and quantify phytoene, carotenoids, and chlorophylls has been detailed by Fraser et al. (2000)
We are grateful to Prof. Dr. C. Wilhelm and Dr. T. Jakob (Leipzig) and Dr. S. Lobréaux (Grenoble) for helpful discussions, and to J.P. Alcaraz (Grenoble) for expert technical assistance. M.S. was supported by the Iranian Ministry of Science, Research, and Technology (Ph.D. scholarship). Received July 26, 2007; accepted September 10, 2007; published September 14, 2007.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Marcel Kuntz (marcel.kuntz{at}ujf-grenoble.fr). www.plantphysiol.org/cgi/doi/10.1104/pp.107.106336 * Corresponding author; e-mail marcel.kuntz{at}ujf-grenoble.fr.
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ABSTRACT
RESULTS
-carotene and traces of other compounds). All pigment levels in gh were reduced to about one-half the amount found in SM. 
