Annals of Botany 89: 833-839, 2002
© 2002 Annals of Botany Company
Rubisco Activity: Effects of Drought Stress
1CPI, IACR-Rothamsted, Harpenden, Herts AL5 2JQ, UK and 2Department of Biological Sciences IENS, Lancaster University, Lancaster LA1 4YQ, UK
* For correspondence. E-mail martin.parry{at}bbsrc.ac.uk
Received: 28 October 2001; Returned for revision: 4 December 2001; Accepted 1 February 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activity is modulated in vivo either by reaction with CO2 and Mg2+ to carbamylate a lysine residue in the catalytic site, or by the binding of inhibitors within the catalytic site. Binding of inhibitors blocks either activity or the carbamylation of the lysine residue that is essential for activity. At night, in many species, 2-carboxyarabinitol-1-phosphate (CA1P) is formed which binds tightly to Rubisco, inhibiting catalytic activity. Recent work has shown that tight-binding inhibitors can also decrease Rubisco activity in the light and contribute to the regulation of Rubisco activity. Here we determine the influence that such inhibitors of Rubisco exert on catalytic activity during drought stress. In tobacco plants, ‘total Rubisco activity’, i.e. the activity following pre-incubation with CO2 and Mg2+, was positively correlated with leaf relative water content. However, ‘total Rubisco activity’ in extracts from leaves with low water potential increased markedly when tightly bound inhibitors were removed, thus increasing the number of catalytic sites available. This suggests that in tobacco the decrease of Rubisco activity under drought stress is not primarily the result of changes in activation by CO2 and Mg2+ but due rather to the presence of tight-binding inhibitors. The amounts of inhibitor present in leaves of droughted tobacco based on the decrease in Rubisco activity per mg soluble protein were usually much greater than the amounts of the known inhibitors (CA1P and ‘daytime inhibitor’) that can be recovered in acid extracts. Alternative explanations for the difference between maximal and total activities are discussed.
Key words: Ribulose bisphosphate carboxylase/oxygenase, Rubisco, water stress, drought, leaf water potential, CO2 assimilation rate, CA1P, regulation.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Drought is a major limitation to the productivity of many crops (Araus et al., 2002; Chaves, 2002; Ober and Luterbacher, 2002). Stomatal closure in response to drought stress restricts CO2 entry into leaves thereby decreasing CO2 assimilation as well as decreasing water loss from the leaves (Cornic, 1994). In addition, there is evidence that the decrease in CO2 assimilation rates found in drought-stressed leaves cannot be simply reversed by increasing the external CO2 supply, showing that drought stress must also affect mesophyll metabolism (Lawlor, 1995, 2002; Cornic and Fresneau, 2002; Tang et al., 2002). This mesophyll response becomes progressively more important with increasing water deficiency (Giménez et al., 1992; Tezara and Lawlor, 1995).
Despite numerous studies, a definitive conclusion as to the most drought-sensitive changes in metabolism remains elusive. However, several studies have suggested that decreased photosynthetic capacity results from impaired regeneration of ribulose-1,5-bisphosphate (RuBP) (Giménez et al., 1992). Whether or not this is a consequence of decreased ATP synthesis is disputed (Gunasekera and Berkowitz, 1993; Tezara et al., 1999). Whilst analysis of transgenic plants with decreased amounts of the CO2 assimilating enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) suggests that Rubisco may not be the main limitation in chloroplast metabolism, the effects of water stress on the amount and activity of Rubisco cannot be ignored. For example, even in the recent study by Tezara et al. (1999) that identified ATP availability as a key feature of drought stress, the changes in ATP were in fact smaller than those for Rubisco at low water potentials, when CO2 assimilation was much decreased.
The amount of Rubisco in leaves is controlled by the rate of synthesis and degradation. Even under drought stress the Rubisco holoenzyme is relatively stable with a half-life of several days (Webber et al., 1994). However, drought stress in tomato (Bartholomew et al., 1991), arabidopsis (Williams et al., 1994) and rice (Vu et al., 1999) leads to a rapid decrease in the abundance of Rubisco small subunit (rbcS) transcripts, which may indicate decreased synthesis.
Rubisco activity is regulated to match the capacity of the leaf to regenerate RuBP, being modulated in vivo either by reaction with CO2 and Mg2+ to carbamylate a lysine residue in the catalytic site, or by the binding of inhibitors within the catalytic site (Parry et al., 1999). The binding of inhibitors to carbamylated Rubisco prevents catalysis, whilst binding of the substrate RuBP to the non-carbamylated enzyme prevents carbamylation of the lysine residue that is essential for activity. The release of such tightly bound compounds requires the participation of Rubisco activase and the hydrolysis of ATP (Salvucci, 1989; Portis, 1995). Whilst measurement of Rubisco activity immediately upon extraction (‘initial activity’) reflects activity in vivo, the carboxylation potential (‘total activity’) can be determined by incubating extracts with high concentrations of CO2 and Mg2+ prior to assay. However, the maximal carboxylation potential (‘maximal activity’) is only revealed if steps are first taken to remove any inhibitors bound to active sites (Parry et al., 1997). Most inhibitors can be removed in vitro by high concentrations of sulfate (Parry et al., 1997).
The short-term responses of Rubisco to drought stress are not clear, as different studies have produced conflicting results. Whereas Giménez et al. (1992) and Gunasekera and Berkowitz (1993), working on sunflower and tobacco, respectively, found little effect of drought on Rubisco, Majumdar et al. (1991) considered loss of Rubisco activity to be a rapid and very early response to drought stress in soybean. Increasing severity and duration of drought stress do, however, decrease both Rubisco activity (Tezara and Lawler, 1995) and protein content (Kicheva et al., 1994) in sunflower and wheat, respectively. However, caution must be exercised when comparing such responses due to the different species and experimental approaches employed.
Under Mediterranean field conditions, Parry et al. (1993) found that the Rubisco activity of tobacco was decreased under drought stress, and proposed that this was caused by the accumulation of tight-binding inhibitors within the catalytic sites. Consistent with this hypothesis was the decrease in Rubisco Kcat (catalytic activity of activated Rubisco expressed per Rubisco molecule) found in subterranean clover grown under drought stress (Medrano et al., 1997). In the present paper we analyse this hypothesis further for tobacco and wheat plants subjected to progressive drought stress.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Materials
RuBP was made enzymically from AMP (Wong et al., 1980). CABP and [2'-14C]CABP were formed by reacting unlabelled or 14C-labelled potassium cyanide (55·1 µCi mol–1; Amersham Pharmacia, Little Chalfont, UK), respectively, with RuBP under weakly alkaline conditions and separating the products as described by Pierce et al. (1980). CA1P and [2'-14C]CA1P were derived from CABP and [2'-14C]CABP, respectively, by limited treatment with potato acid phosphatase; phosphatase activity being terminated once 50 % of the organic phosphate had been released as orthophosphate (Gutteridge et al., 1989).
Plant culture
Individual tobacco plants (cultivar Samsun) were grown in 20 cm diameter pots in a controlled environment (25 °C day/20 °C night, 300 µmol m–2 s–1, 14 h photoperiod). When the plants had approx. eight fully expanded leaves, drought stress was imposed by withholding water over a period of up to 10 d. Samples were taken every other day 9 h into the light period from the three uppermost fully expanded leaves for both control and droughted plants. Leaf discs, 2·7 cm in diameter, were taken using a corkborer for the determination of relative water content (RWC), Rubisco activity and amount, and inhibitor content (freeze clamp).
Six wheat plants (cultivar Riband) were grown in each 20 cm diameter pot in a controlled environment (Sparks et al., 2001) (18 °C day/15 °C night, 600 µmol m–2 s–1, 16 h photoperiod). Wheat was droughted for 10 d by withholding water at ear emergence. Samples were taken 10 h into the light period from both control and droughted plants. Leaf discs of 1·0 cm diameter were taken using a corkborer for determination of RWC, Rubisco activity and abundance, and inhibitor content (freeze clamp).
Plant water status
The RWC of leaves was determined using the formula:
RWC = 100 [(MF – MD)/(MT – MD)]
where MF, MD and MT are fresh, dry and turgid masses of the sampled leaf, respectively.
Biochemical determinations
For measurements of Rubisco activity, frozen leaf discs were ground to a fine powder in liquid nitrogen and rapidly extracted with 2·0 ml ice-cold extraction buffer containing 50 mM Bicine, pH 8·0, 20 mM MgCl2, 2 mM phenylmethlysulfonyl fluoride, 50 mM 2-mercaptoethanol and 30 mg polyvinylpolypyrrolidone (PVPP). The extracts were clarified by centrifugation (10 000 g at 4 °C for 2 min) and the initial, total and maximum Rubisco activity determined according to Parry et al. (1997). Soluble protein was determined according to the method of Bradford (1976).
The buffered extract (0·45 ml) was added to 0·1 ml of concentrated 99 % trifluoracetic acid (TFA) as soon as possible after extraction, vortexed and stored frozen in the supernatant prior to inhibitor quantification. The amounts of Rubisco inhibitor were determined according to Keys et al. (1995) by the extent of inhibition of Rubisco activity in a two-stage assay.
For characterization of tight-binding inhibitors by high performance liquid chromatography, leaf samples were extracted directly with 3·5 % (v/v) TFA and the extracts purified by passage through C18 and Dowex 50 columns as described by Andralojc et al. (1994). Direct extraction of the tissue with acid was also used in the preparation of samples for assay of inhibitors by the extent of inhibition of Rubisco activity. For this, residues from the acid extract were assayed directly for the daytime inhibitor, while CA1P was measured after pre-incubation of residues in Tris–HCl buffer pH 8·2 to destroy the daytime inhibitor and to hydrolyse CA1P lactone to the inhibitory acid.
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RESULTS |
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Tobacco
Following drought treatments, the RWC of tobacco leaves ranged from 47 % in the most severely droughted plants to 80 % in well-watered plants (Fig. 1). Initial (Fig. 1A) and total (Fig. 1B) Rubisco activities were strongly correlated with leaf relative water content (P < 0·001). In contrast, maximal activities were only weakly correlated with RWC (Fig. 1C).
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Total and maximal Rubisco activities were used to estimate the percentage of catalytic sites that were blocked by inhibitors. This derivative is based on the assumption that the maximal activity represented the true catalytic capacity of the enzyme and that activities less than this value varied linearly with the proportion of catalytic sites containing Rubisco inhibitor. There was a significant (P < 0·01) negative correlation between the estimate of inhibited catalytic sites and RWC (Fig. 2A). However, the scatter of points was considerable (Fig. 2A). Furthermore, as RWC declined so did the amount of Rubisco (Fig. 2B).
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The inhibitory components in TFA extracts taken in parallel were separated by ion exchange HPLC and individual fractions tested for their ability to inhibit Rubisco. All of the samples tested contained fractions with modest inhibitory activity with a retention time of 18 min, consistent with CA1P (Fig. 3A and B). In addition, some stressed samples contained another inhibitory compound (Fig. 3B). This had a much longer retention time of 22·5 min, consistent with a bisphosphate and similar to that of the ‘daytime inhibitor’ reported by Parry et al. (1997).
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To obtain better evidence for the involvement of known inhibitors in the loss of Rubisco activity during drought stress, subsamples from bulked leaf material from droughted and non-droughted plants were analysed (Table 1). A decrease in initial and total activities of Rubisco was shown with increasing drought stress. This cannot readily be explained by the amount of daytime inhibitor, since this decreased in leaves with the lowest RWC. Furthermore, the amounts of daytime inhibitor are insufficient to account for the number of sites inhibited, as estimated from total and maximal activities. There was, however, an increase in CA1P in this tissue to 5·3 nmol g–1 f. wt. This is of the right order of magnitude to explain the difference between total and maximal activities for this sample, with 1·82 mg Rubisco protein g–1 f. wt. This experiment shows that using a range of leaves of varying physiological age, there was a loss of Rubisco protein with increasing drought. This may reflect accelerated senescence in the older leaves of plants, caused by drought. The decreased soluble protein content is also consistent with this explanation.
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Wheat
Following drought treatments, RWC in wheat leaves ranged from 67 % in the most severely droughted plants to 97 % in well-watered plants (Fig. 4). Within this range of RWC both total (Fig. 4A) and maximal (Fig. 4B) Rubisco activities were poorly correlated with leaf relative water content. In addition, there was no significant correlation between the percentage of catalytic sites that were blocked by inhibitors and RWC (Fig. 4C). However, blockage of 10–60 % of the catalytic sites (Fig. 4C) indicated the presence of substantial amounts of inhibitor, and yet the supernatant from acidified buffer extracts did not contain sufficient amounts of Rubisco inhibitor to explain the calculated number of blocked sites (data not shown).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The extent and rate of change in RWC were as expected for tobacco and wheat plants grown for up to 10 d without water. In tobacco, drought decreased the initial and total activities of Rubisco. The decrease in activity appears to result primarily from a decrease in the apparent Kcat rather than from a change in the activation state. Similar decreases in Rubisco Kcat in response to long-term drought stress have been reported for field-grown tobacco (Parry et al., 1993) and subterranean clover (Medrano et al., 1997).
Maximal activities were only weakly correlated (tobacco; Fig. 1C) with RWC, or not correlated at all (wheat; Fig 4B), suggesting either limited irreversible damage to Rubisco, or a decrease in its contribution to the total amount of soluble protein (since activities are expressed relative to soluble protein). Severe drought is known to decrease the amounts of Rubisco protein in some other species (Majumdar et al., 1991).
In both tobacco (Fig. 1) and wheat (Fig. 4), the total activity is almost always lower than the corresponding maximal activity for all values of RWC, indicating the presence of tightly bound inhibitors. Full catalytic activity can be restored in vitro by treatment with sulfate or in vivo by the ancillary enzyme Rubisco activase. Such inhibition is therefore considered to be reversible.
However, the amounts of CA1P, the best characterized naturally occurring tight-binding inhibitor (Gutteridge et al., 1986; Berry et al., 1987), were not consistently increased under drought (Table 1). The amounts of an alternative tight-binding inhibitor, which was chromatographically indistinguishable from the daytime inhibitor first reported by Keys et al. (1995), were not sufficient to account for the differences between total and maximal Rubisco activities. The daytime inhibitor appears not to be confined to those species that produce CA1P (Parry et al., 1997). Since it also shares many properties in common with D-glycero-2,3-pentodiulose-1,5-bisphosphate (PDBP) (Kane et al., 1998), a product of RuBP oxidation, it may be an inevitable and ubiquitous derivative of the substrate RuBP. The binding of the Rubisco inhibitor, CA1P, to Rubisco has been shown to protect the enzyme from proteolytic degradation (Khan et al., 1999). Rubisco actively engaged in the carboxylation of RuBP is relatively resistant to protease degradation; conversely, uncarbamylated Rubisco with vacant catalytic sites is very susceptible to proteolysis. Such interactions of Rubisco with tight-binding inhibitors may be advantageous in vivo as they could prevent Rubisco that is not being used for catalysis from being degraded by proteases.
The release of tight-binding inhibitors requires the participation of Rubisco activase and the hydrolysis of ATP (Salvucci, 1989; Portis, 1995). The removal of inhibitors by Rubisco activase may be impaired because concentrations of ATP are decreased by drought (Lawlor, 1995; Tezara et al., 1999). In addition, Rubisco activase is susceptible to the high temperatures (Crafts-Brandner and Salvucci, 2000) that may be associated with drought stress. However, any impairment of Rubisco activase function must be partial since when samples were taken in the latter part of the photoperiod in these experiments, there was little evidence to suggest that CA1P produced during a previous period of darkness was still bound to Rubisco. Thus, Rubisco activase must have been effective at some stage during the day.
Because the ‘daytime inhibitor’ was first described in wheat, we also investigated the effect of drought on Rubisco activity in wheat (Fig. 4). Interestingly, decreases in RWC similar to those occurring in tobacco had little effect on Rubisco total activity. Furthermore, decreased RWC did not lead to increased amounts of tight-binding inhibitors in acid extracts. This result contradicts indirect estimates of the percentage of catalytic sites blocked by inhibitors (calculated from total and maximal activities), which suggested that a large number of sites should be blocked by inhibitors. This discrepancy must be accounted for by other factors as wheat does not contain large amounts of CA1P (Servaites et al., 1986).
Holaday et al. (1992) found that total Rubisco activity of wheat flag leaves was decreased when drought stress was applied at anthesis. This decrease was accompanied by a decrease in both soluble protein and chlorophyll. Data in Fig. 4 refer to wheat flag leaves at, or soon after, ear emergence, when the flag leaf was quite young. It seems that decreases in total Rubisco activity per mg soluble protein may be partly explained by a loss of Rubisco protein during leaf drought stress; this additional effect of physiological age needs further study. There are two other mechanisms to be considered. First, Rubisco readily reverts to a slow activating state in vitro by conformational change (Gutteridge et al., 1982; Schmidt et al., 1984). The possibility of this mechanism having a regulatory role in vivo has received little attention and poses problems for the investigator. The second possibility is the inhibition of Rubisco by RuBP binding to non-carbamylated sites. This mechanism has been regarded as especially relevant to activation by Rubisco activase, the assay of which utilizes Rubisco that has been decarbamylated, treated with RuBP and stored at low temperature (Robinson et al., 1988; Salvucci, 1992). It is of interest that these conditions would also result in the conversion of rapidly activating Rubisco to the slowly activating form and the generation of inhibitory RuBP derivatives (Kane et al., 1998). How drought stress affects the expression and activity of Rubisco activase in wheat has yet to be determined. However, Rubisco activase expression is increased in wheat under heat stress (Law and Crafts-Brandner, 2001)
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ACKNOWLEDGEMENT |
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IACR-Rothamsted is a grant-aided institute of the BBSRC.
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 N. Hirotsu, A. Makino, S. Yokota, and T. Mae The Photosynthetic Properties of Rice Leaves Treated with Low Temperature and High Irradiance Plant Cell Physiol., August 1, 2005; 46(8): 1377 - 1383. [Abstract] [Full Text] [PDF]
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H. GRIFFITHS and M. A. J. PARRY Plant Responses to Water Stress Ann. Bot., June 15, 2002; 89(7): 801 - 802. [Abstract] [Full Text] [PDF]
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D. W. LAWLOR Limitation to Photosynthesis in Water-stressed Leaves: Stomata vs. Metabolism and the Role of ATP Ann. Bot., June 15, 2002; 89(7): 871 - 885. [Abstract] [Full Text] [PDF]
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H. MEDRANO, J. M. ESCALONA, J. BOTA, J. GULIAS, and J. FLEXAS Regulation of Photosynthesis of C3 Plants in Response to Progressive Drought: Stomatal Conductance as a Reference Parameter Ann. Bot., June 15, 2002; 89(7): 895 - 905. [Abstract] [Full Text] [PDF]
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